Roger T. Hanlon

Cephalopod dynamic camouflage.

Everyone knows what camouflage is and how it works. And many people (some scientists included) think chameleons are the masters of color change. Wrong on both counts. In this primer, I provide an overview of recent work on the mechanisms and principles of rapid adaptive camouflage of cephalopods — octopus, cuttlefish and squids. These strange but capable marine invertebrates can camouflage themselves against almost any background, a feat well appreciated by Aristotle, and one never mastered by any land animal.

Mechanisms and behavioural functions of structural coloration in cephalopods

Octopus, squid and cuttlefish are renowned for rapid adaptive coloration that is used for a wide range of communication and camouflage. Structural coloration plays a key role in augmenting the skin patterning that is produced largely by neurally controlled pigmented chromatophore organs. While most iridescence and white scattering is produced by passive reflectance or diffusion, some iridophores in squid are actively controlled via a unique cholinergic, non-synaptic neural system. We review the recent anatomical and experimental evidence regarding the mechanisms of reflection and diffusion of light by the different cell types (iridophores and leucophores) of various cephalopod species. The structures that are responsible for the optical effects of some iridophores and leucophores have recently been shown to be proteins. Optical interactions with the overlying pigmented chromatophores are complex, and the recent measurements are presented and synthesized. Polarized light reflected from iridophores can be passed through the chromatophores, thus enabling the use of a discrete communication channel, because cephalopods are especially sensitive to polarized light. We illustrate how structural coloration contributes to the overall appearance of the cephalopods during intra- and interspecific behavioural interactions including camouflage.

Polarization vision helps detect transparent prey

Transparency enables aquatic organisms to avoid detection by visual predators. But we have found that this camouflage can be broken using a visual mode evolved by several predators, such as squid. Under partially linearly polarized lighting, squid detect zooplankton prey at a distance 70% greater than those achieved under non-polarized illumination. The role of polarization sensitivity in predation is confirmed by squids preference for transparent, yet polarization-active, targets that mimic their prey.

Cephalopod dynamic camouflage: bridging the continuum between background matching and disruptive coloration

Individual cuttlefish, octopus and squid have the versatile capability to use body patterns for background matching and disruptive coloration. We define—qualitatively and quantitatively—the chief characteristics of the three major body pattern types used for camouflage by cephalopods: uniform and mottle patterns for background matching, and disruptive patterns that primarily enhance disruptiveness but aid background matching as well. There is great variation within each of the three body pattern types, but by defining their chief characteristics we lay the groundwork to test camouflage concepts by correlating background statistics with those of the body pattern. We describe at least three ways in which background matching can be achieved in cephalopods. Disruptive patterns in cuttlefish possess all four of the basic components of ‘disruptiveness’, supporting Cotts hypotheses, and we provide field examples of disruptive coloration in which the body pattern contrast exceeds that of the immediate surrounds. Based upon laboratory testing as well as thousands of images of camouflaged cephalopods in the field (a sample is provided on a web archive), we note that size, contrast and edges of background objects are key visual cues that guide cephalopod camouflage patterning. Mottle and disruptive patterns are frequently mixed, suggesting that background matching and disruptive mechanisms are often used in the same pattern.

Cuttlefish use polarization sensitivity in predation on silvery fish

Cephalopods are sensitive to the linear polarization characteristics of light. To examine if this polarization sensitivity plays a role in the predatory behavior of cuttlefish, we examined the preference of Sepia officinalis when presented with fish whose polarization reflection was greatly reduced versus fish whose polarization reflection was not affected. Cuttlefish preyed preferably on fish with normal polarization reflection over fish that did not reflect linearly polarized light (n = 24, chi 2 = 17.3, P < 0.0001), implying that polarization sensitivity is used during predation. We suggest that polarization vision is used to break the countershading camouflage of light-reflecting silvery fish.

Effect of temperature on laboratory growth, reproduction and life span of Octopus bimaculoides

Laboratory culture of 40 Octopus bimaculoides from April 1982 to August 1983 through the full life cycle at 18°C vs 23°C provided information on the growth, reproductive biology and life span of this California littoral octopus. At 18°C, the cephalopods grew from a hatchling size of 0.07 g to a mean of 619 g in 404 d; the largest individual was 872 g. Octopuses cultured at 23°C reached their highest mean weight of 597 g in 370 d; the largest individual grown at this temperature was 848 g after 404 d. Growth data revealed a two-phase growth pattern: a 5 mo exponential phase followed by a slower logarithmic (power function) phase until spawning. At 5 mo octopuses grown at 23°C were over three times larger than their 18°C siblings. However, beyond 6.5 mo, growth rates were no higher at 23°C than at 18°C. At 13.5 mo, the mean weight of the 18°C group surpassed that of the 23°C group. The slope of the length/weight (L/W) relationship was significantly different for the two temperature regimes, with the 23°C octopuses weighing 18% less than their 18°C siblings at a mantle length of 100 mm. Females weighed more than males at any given mantle length. Males grew slightly larger and matured before females. The L/W relationship indicated isometric body growth throughout the life cycle. Higher temperature accelerated all aspects of reproductive biology and shortened life span by as much as 20% (from approximately 16 to 13 mo). O. bimaculoides has one of the longest life cycles among species with large eggs and benthic hatchlings. Extrapolations to field growth are made, and the possible effects of temperature anomalies such as El Niño are discussed.

Adaptive optoelectronic camouflage systems with designs inspired by cephalopod skins.

Significance Artificial systems that replicate functional attributes of the skins of cephalopods could offer capabilities in visual appearance modulation with potential utility in consumer, industrial, and military applications. Here we demonstrate a complete set of materials, components, fabrication approaches, integration schemes, bioinspired designs, and coordinated operational modes for adaptive optoelectronic camouflage sheets. These devices are capable of producing black-and-white patterns that spontaneously match those of the surroundings, without user input or external measurement. Systematic experimental, computational, and analytical studies of the optical, electrical, thermal, and mechanical properties reveal the fundamental aspects of operation and also provide quantitative design guidelines that are applicable to future embodiments. Octopus, squid, cuttlefish, and other cephalopods exhibit exceptional capabilities for visually adapting to or differentiating from the coloration and texture of their surroundings, for the purpose of concealment, communication, predation, and reproduction. Long-standing interest in and emerging understanding of the underlying ultrastructure, physiological control, and photonic interactions has recently led to efforts in the construction of artificial systems that have key attributes found in the skins of these organisms. Despite several promising options in active materials for mimicking biological color tuning, existing routes to integrated systems do not include critical capabilities in distributed sensing and actuation. Research described here represents progress in this direction, demonstrated through the construction, experimental study, and computational modeling of materials, device elements, and integration schemes for cephalopod-inspired flexible sheets that can autonomously sense and adapt to the coloration of their surroundings. These systems combine high-performance, multiplexed arrays of actuators and photodetectors in laminated, multilayer configurations on flexible substrates, with overlaid arrangements of pixelated, color-changing elements. The concepts provide realistic routes to thin sheets that can be conformally wrapped onto solid objects to modulate their visual appearance, with potential relevance to consumer, industrial, and military applications.

Malleable skin coloration in cephalopods: selective reflectance, transmission and absorbance of light by chromatophores and iridophores

Nature’s best-known example of colorful, changeable, and diverse skin patterning is found in cephalopods. Color and pattern changes in squid skin are mediated by the action of thousands of pigmented chromatophore organs in combination with subjacent light-reflecting iridophore cells. Chromatophores (brown, red, yellow pigment) are innervated directly by the brain and can quickly expand and retract over underlying iridophore cells (red, orange, yellow, green, blue iridescence). Here, we present the first spectral account of the colors that are produced by the interaction between chromatophores and iridophores in squid (Loligo pealeii). Using a spectrometer, we have acquired highly focused reflectance measurements of chromatophores, iridophores, and the quality and quantity of light reflected when both interact. Results indicate that the light reflected from iridophores can be filtered by the chromatophores, enhancing their appearance. We have also measured polarization aspects of iridophores and chromatophores and show that, whereas structurally reflecting iridophores polarize light at certain angles, pigmentary chromatophores do not. We have further measured the reflectance change that iridophores undergo during physiological activity, from “off” to various degrees of “on”, revealing specifically the way that colors shift from the longer end (infra-red and red) to the shorter (blue) end of the spectrum. By demonstrating that three color classes of pigments, combined with a single type of reflective cell, produce colors that envelop the whole of the visible spectrum, this study provides an insight into the optical mechanisms employed by the elaborate skin of cephalopods to give the extreme diversity that enables their dynamic camouflage and signaling.

Sound detection by the longfin squid (Loligo pealeii) studied with auditory evoked potentials: sensitivity to low-frequency particle motion and not pressure

SUMMARY Although hearing has been described for many underwater species, there is much debate regarding if and how cephalopods detect sound. Here we quantify the acoustic sensitivity of the longfin squid (Loligo pealeii) using near-field acoustic and shaker-generated acceleration stimuli. Sound field pressure and particle motion components were measured from 30 to 10,000 Hz and acceleration stimuli were measured from 20 to 1000 Hz. Responses were determined using auditory evoked potentials (AEPs) with electrodes placed near the statocysts. Evoked potentials were generated by both stimuli and consisted of two wave types: (1) rapid stimulus-following waves, and (2) slower, high-amplitude waves, similar to some fish AEPs. Responses were obtained between 30 and 500 Hz with lowest thresholds between 100 and 200 Hz. At the best frequencies, AEP amplitudes were often >20 μV. Evoked potentials were extinguished at all frequencies if (1) water temperatures were less than 8°C, (2) statocysts were ablated, or (3) recording electrodes were placed in locations other than near the statocysts. Both the AEP response characteristics and the range of responses suggest that squid detect sound similarly to most fish, with the statocyst acting as an accelerometer through which squid detect the particle motion component of a sound field. The modality and frequency range indicate that squid probably detect acoustic particle motion stimuli from both predators and prey as well as low-frequency environmental sound signatures that may aid navigation.

Biological Characteristics and Biomedical Applications of the Squid Sepioteuthis lessoniana Cultured Through Multiple Generations

Providing squids--especially their giant axons--for biomedical research has now been achieved in 10 mariculture trials extending through multiple generations. The noteworthy biological characteristics of Sepioteuthis lessoniana are (1) this species is behaviorally and morphologically well suited to the laboratory environment; (2) the life cycle is completed in 4-6 months; (3) growth is rapid (12% and 5% wet body weight d-1 for 100 d and for the life span, respectively), with adult size ranging from 0.4-2.2 kg; (4) feeding rates are high (30% wet body weight d-1), and a variety of live crustaceans and fishes are eaten; (5) crowding is tolerated (about 4 squids m-3); (6) the incidence of disease and cannibalism is low; and (7) reproduction in captivity allows culture through three successive generations. Engineering factors contributed to culture success: (1) physical design (i.e., size, shape, and painted pattern) of the culture tanks; (2) patterns of water flow in the culture tanks; (3) water filtration systems; and (4) spawning substrates. Initial production (a few hundred squids per year) suggests that large-scale culture will be able to supply the needs of the biomedical research community. The size (> 400 microns in diameter) and characteristics of the giant axons of Sepioteuthis are appropriate for experimentation, and other studies indicate that the eye, oculomotor/equilibrium system, olfactory system, blood, and ink are equally suitable for research.