Elaborate pupils in skates may help camouflage the eye

Author Posting. © Company of Biologists, 2019. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 222 (2019): jeb195966, doi:10.1242/jeb.195966.The skate Leucoraja erinacea is a bottom-dweller that buries into the substrate with its eyes protruding, revealing elaborately shaped pupils. It has been suggested that such pupil shapes may camouflage the eye, yet this has never been tested. Here, we asked whether skate pupils dilate or constrict depending on background spatial frequency. In experiment 1, the skates' pupillary response to three artificial checkerboards of different spatial frequencies was recorded. Results showed that pupils did not change in response to spatial frequency. In experiment 2, in which skates buried into three natural substrates of different spatial frequencies, such that their eyes protruded, pupils showed a subtle but statistically significant response to changes in substrate spatial frequency. Although light intensity is the primary factor determining pupil dilation, our results show that pupils also change depending on the spatial frequency of natural substrates, which suggests that pupils may aid in camouflaging the eye.This work was funded by awards from the Marine Biological Laboratory (specifically, the Hermann Foundation Award, Joan Ruderman Fund Award, Grass Foundation Fund Award and Neal Cornell Career Development Award), as well as a University of Chicago Metcalf Fellowship to C.O.2020-01-2

Cuttlefish camouflage: The effects of substrate contrast and size in evoking uniform, mottle or disruptive body patterns

AbstractCuttlefish are cephalopod molluscs that achieve dynamic camouflage by rapidly extracting visual information from the background and neurally implementing an appropriate skin (or body) pattern. We investigated how cuttlefish body patterning responses are influenced by contrast and spatial scale by varying the contrast and the size of checkerboard backgrounds. We found that: (1) at high contrast levels, cuttlefish body patterning depended on check size; (2) for low contrast levels, body patterning was independent of “check” size; and (3) on the same check size, cuttlefish fine-tuned the contrast and fine structure of their body patterns, in response to small contrast changes in the background. Furthermore, we developed an objective, automated method of assessing cuttlefish camouflage patterns that quantitatively differentiated the three body patterns of uniform/stipple, mottle and disruptive. This study draws attention to the key roles played by background contrast and particle size in determining an effective camouflage pattern

Changes in reflectin protein phosphorylation are associated with dynamic iridescence in squid

Author Posting. © The Author(s), 2009. This is the author's version of the work. It is posted here by permission of The Royal Society for personal use, not for redistribution. The definitive version was published in Journal of The Royal Society Interface 6 (2010): 549-560, doi:10.1098/rsif.2009.0299.Many cephalopods exhibit remarkable dermal iridescence, a component of their complex, dynamic camouflage and communication. In the species Euprymna scolopes, the light-organ iridescence is static and is due to reflectin protein-based platelets assembled into lamellar thin-film reflectors called iridosomes, contained within iridescent cells called iridocytes. Squid in the family Loliginidae appear to be unique in that the dermis possesses a dynamic iridescent component, with reflective, colored structures that are assembled and disassembled under the control of the muscarinic cholinergic system and the associated neurotransmitter acetylcholine (Mathger et al. 2004). Here we present the sequences and characterization of three new members of the reflectin family associated with the dynamically changeable iridescence in Loligo and not found in static Euprymna iridophores. In addition, we show that application of genistein, a protein tyrosine kinase inhibitor, suppresses acetylcholine- and calcium-induced iridescence in Loligo. We further demonstrate that two of these novel reflectins are extensively phosphorylated in concert with the activation of iridescence by exogenous acetylcholine. This phosphorylation and the correlated iridescence can be blocked with genistein. Our results suggest that tyrosine phosphorylation of reflectin proteins is involved in the regulation of dynamic iridescence in Loligo.We gratefully acknowledge support from Anteon contract F33615-03-D-5408 to the Marine Biological Laboratory, Woods Hole, MA and grant # W911NF-06-1-0285 from the Army Research Office to D.E.M

The response of squid and fish to changes in the angular distribution of light

This paper describes the responses of a squid (Alloteuthis subulata) and a fish (Trachurus trachurus) to changes in the angular distribution of light. An apparatus was made that simulated the angular distribution of daylight in the sea. The apparatus enabled the direction of the brightest light to be changed and the positions of the animals in response to these changes were observed. Squid viewed head-on were observed to roll by a maximum of 20° when the incident light source was at angles between 20° and 90° (where 0° is vertically downwards). When viewed laterally, i.e. in the pitch plane, the squid were observed to position themselves more closely with respect to the angle of the light source, they swam in a near vertical plane when the incident light source was at an angle of 90°. Swimming movements in the roll and pitch plane became more horizontal with positions of the light source between 90 and 180°. Horse mackerel, in contrast, inclined their dorsal surfaces to almost perfectly match the angle of the incident light source, even swimming upside-down when light came from below. These experiments also revealed that squid display a counter-shading chromatophore pattern ('Flexible Countershading') in response to light coming from the sides, which involves darkening the side of the body facing the brightest light. The use of chromatophores in this way may explain why the dorsal light reflex in squid is so weak compared to that of fish

Anatomical basis for camouflaged polarized light communication in squid

Camouflage is a means to defeat visual detection by predators, whereas visual communication involves a signal that is conspicuous to a receiver (usually a conspecific). However, most intraspecific visual signals are also conspicuous to predators, so that signalling can lead to the serious consequence of predation. Could an animal achieve visual camouflage and simultaneously send a hidden visual message to a conspecific? Here, we present evidence that the polarized aspect of iridescent colour in squid skin is maintained after it passes through the overlying pigmented chromatophores, which produce the highly evolved—and dynamically changeable—camouflaged patterns in cephalopods. Since cephalopods are polarization sensitive, and can regulate polarization via skin iridescence, it is conceivable that they could send polarized signals to conspecifics while staying camouflaged to fish or mammalian predators, most of which are not polarization sensitive

Data from: Changeable camouflage: how well can flounder resemble the colour and spatial scale of substrates in their natural habitats?

Flounder change colour and pattern for camouflage. We used a spectrometer to measure reflectance spectra and a digital camera to capture body patterns of two flounder species camouflaged on four natural backgrounds of different spatial scale (sand, small gravel, large gravel and rocks). We quantified the degree of spectral match between flounder and background relative to the situation of perfect camouflage in which flounder and background were assumed to have identical spectral distribution. Computations were carried out for three biologically relevant observers: monochromatic squid, dichromatic crab and trichromatic guitarfish. Our computations present a new approach to analysing datasets with multiple spectra that have large variance. Furthermore, to investigate the spatial match between flounder and background, images of flounder patterns were analysed using a custom program originally developed to study cuttlefish camouflage. Our results show that all flounder and background spectra fall within the same colour gamut and that, in terms of different observer visual systems, flounder matched most substrates in luminance and colour contrast. Flounder matched the spatial scales of all substrates except for rocks. We discuss findings in terms of flounder biology; furthermore, we discuss our methodology in light of hyperspectral technologies that combine high-resolution spectral and spatial imaging

The role of muscarinic receptors and intracellular Ca2+ in the spectral reflectivity changes of squid iridophores

In this paper we describe changes in spectral reflectivity of the light reflectors (iridophores) of the squid Alloteuthis subulata. The spectral changes that can be seen in living squid, can also be brought about by superfusing whole skin preparations with acetylcholine (ACh) (20 μmol l) and muscarine (30 μmol l) but not nicotine (up to 50 mmol l ), suggesting that cholinergic muscarinic receptors are involved. Changing the osmolarity of the external solution had no effect on spectral reflectivity. To study the iridophores at the cellular level, iridophores were isolated enzymatically. Lucifer Yellow filled the iridophores uniformly, showing cellular individuality. Isolated iridophore cells were loaded with Fura-2 AM and cytoplasmic Ca was recorded ratiometrically. Intracellular Ca (resting concentration at 66.16 nmol l) increased transiently after addition of ACh (50 μmol l), muscarine (25 μmol l), but not nicotine (up to 5 mmol l). Ca also increased when superfused with potassium chloride (10 mmol l) and caffeine (2.5 mmol l). Hypo- and hyperosmotic solutions had no effects on the cytoplasmic Ca. By presenting direct evidence that iridophores are polarised cellular structures containing Ca stores and that they are activated via cholinergic muscarinic receptors, we demonstrate that Ca is involved in the reflectivity changes of the iridophores of A. subulata. Specimens were prepared for transmission electron microscopy. It was found that the orientations of the plates with respect to the skin surface are in good agreement with the expected orientations based on the prediction that the iridophores act as multilayer reflectors

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

Spectral and spatial properties of polarized light reflections from the arms of squid (Loligo pealeii) and cuttlefish (Sepia officinalis L.)

On every arm of cuttlefish and squid there is a stripe of high-reflectance iridophores that reflects highly polarized light. Since cephalopods possess polarization vision, it has been hypothesized that these polarized stripes could serve an intraspecific communication function. We determined how polarization changes when these boneless arms move. By measuring the spectral and polarizing properties of the reflected light from samples at various angles of tilt and rotation, we found that the actual posture of the arm has little or no effect on partial polarization or the e-vector angle of the reflected light. However, when the illumination angle changed, the partial polarization of the reflected light also changed. The spectral reflections of the signals were also affected by the angle of illumination but not by the orientation of the sample. Electron microscope samples showed that these stripes are composed of several groups of multilayer platelets within the iridophores. The surface normal to each group is oriented at a different angle, which produces essentially constant reflection of polarized light over a range of viewing angles. These results demonstrate that cuttlefish and squid could send out reliable polarization signals to a receiver regardless of arm orientation