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Sunday, February 1, 2009

Cephalopod-tastic Friday

ResearchBlogging.orgRoger Hanlon, from the Woods Hole Marine Biological Laboratory, came out to UCONN's Avery Point campus to present for our Friday seminar series. His presentation was a good overview of his lab's work on cephalopod camouflage behavior over the past decades, with the majority of the discussion on the work they have done recently with the cuttlefish Sepia officinalis. So I hope you will bear with me while I gush on a bit about my favorite group of animals and their amazing adaptations, which allow them to confound predator, prey, and researchers alike!

One of the first videos (of many) presented was one which leaked to YouTube in low res, but, of course, Roger had it in full resolution and projected large. The video is a magnificent example of high-fidelity camouflage by the octopus employing all its tricks. I've seen an octopus disappear in front of my eyes only once and it was simply amazing. I've seen Roger's video three or four times in high resolution, and each time I get the same wonder-filled reaction. I've probably seen it a hundred times in YouTube's low resolution and even there it makes me pause. For some reason the majority of people who view this think the tricks in the video are in post production not from the octopus...go figure.

Where's the octopus?
Image copyright Roger Hanlon


After the "Wow" example, Roger gave an overview of camouflage related capabilities and systems in cephalopods. He outlined their amazing skin with its dense network of chromatophores and their controlling muscles, underlying irridiphores and leucophores and their muscles, the base skin layer, and the vision and neural control system which allow the cephalopods to coordinate and change all of these structures along with changes in the texture of the skin as fast as they do.


He broadly covered the use of color and patterns in cephalopods for communication, especially in sexual competition and courtship. Regretfully, he ran out of time at the end and didn't cover the wonderful tale of "cross-dressing" cuttlefish males and their success in tricking dominant males to think they are females. His lab also found that females showed a preferential choice of the "cross-dressing" male's sperm for fertilization of the eggs (Hanlon et al. 2005). But, he did show Caribbean reef squid males showing their "two-faced nature", always presenting the female they are wooing with a peaceful calm side, while showing all other squid an extremely aggressive countenance.

Two frames about 10 seconds apart from video by Roger Hanlon. In the first image the male is on the left of the female, showing her a calm, courting display. The stark white display facing away from the female is an aggressive display, warning other males to keep away. In the second frame the male has switched to the right side of the female when she moved and changed his color patterns to keep the docile pattern visible to the female and the aggressive warning showing outward to any other males. Total color change occurred in ~2 seconds.
Images from video, copyright Roger Hanlon


Once Hanlon laid the background information, which was especially important since his audience included physicists, chemists, biologists, and students ranging from age 8 to 70+, Roger moved on to the main focus of his lab's recent work: camouflage. While the octopus in the image at the top is a high-fidelity example of cephalopod camouflage, a near exact match to the background in color, pattern, and texture, in years of observing cephalopods with many thousands of video and photographic records as data points, Hanlon's lab has found that this high-fidelity form of camouflage is very rare. "Good enough" camouflage patterns are far more common. Most of the camouflage in cephalopods can be categorized into 3 broad templates (with variations) of patterning: a fine-grained, average intensity uniform pattern, a medium-grained varied contrast mottled pattern, and large-grained high contrast disruptive pattern. Using their visual records and captive cuttlefish, they have examined these templates extensively.

Each template is used in different circumstances and, with minor variation in pattern and the addition of color matching, is very effective in fooling the eye without having to exactly match the background. In a large variety of controlled tests his team has gradually narrowed in on the base templates and the cues that cuttlefish use to determine which pattern to utilize. The lab uses tanks with natural or laminated backgrounds placed at the bottom of the tank. They capture the reaction of the cuttlefish when the environment is changed using both HD video and still photography. To better quantify the results, they have been using black and white checkerboard and pixilated background patterns with varying sized squares.

The cuttlefish have an area on the top of their mantle that is referred to as the "White Square component" which is characteristically displayed in disruptive camouflage and is proportional to the size of the animal. It is also, even though not visible to the cuttlefish, key in the choice of disruptive camouflage by the cuttlefish.

Disruptive skin components of cuttlefish Sepia officinalis, including the "white Square Component" indicated by the number 2 at the joint of the "T" formation in the left figure. On the right is the result of comparing various sized cuttlefish with various sized grid patterns. At all sizes when the area of one square of the grid is between 40 and 120% of the area of the cuttlefishes white square component, it will utilize the disruptive camouflage. Below and above those relative sizes and the animal moves to mottled or uniform patterning.
From Barbosa et al. (2007).


In their recent research, the lab found that when presented any cue for disruptive patterning, even if it represents only a small percentage of the total environmental cues, e.g. two or three white rocks on sandy bottom, a cuttlefish will choose to move to the cue item and employ a disruptive pattern of camouflage. Interestingly, white pebbles cued the disruptive pattern, but black pebbles did not. They have also determined that the shape of the cue is not critical, but the area is.

In a recent paper, Barbosa, Litman, and Hanlon, set up both vertical and horizontal patterns to test the cuttlefish response against. Since cuttlefish are generally benthic, ideally they must remain camouflaged against predators from above (such as those pesky dolphins) and from the sides simultaneously. In these tests the cuttlefish appeared to weigh the patterns on the side of the tank over the bottom of the tank for choosing their pattern, but they also modified that choice by the bottom pattern. In their quantitative analysis it was found that there was a statistically significant difference between when the side or the bottom only were checkered and between when the bottom was checkered and both the bottom and side were checkered. These differences were displayed in three of eleven discrete skin regions of the cuttlefish.

What happens when the vertical and horizontal patterns are radically different? Qualitatively, the cuttlefish appear to weigh the vertical visual cues over the bottom cues slightly. Quantitatively this is born out in only three areas of the cuttlefish's body.
Figures from Barbosa et al. (2008)


The team at the MBL, having made progress on the cues for disruptive patterning camouflage, is also looking into the effects of substrate contrast and size for uniform, mottled, or disruptive body patterns. For this work they have turned to image processing to grade and analyze the cuttlefish responses to varying check sizes, as before, but also with varying contrast between the check patterns. As with the previous experiments with black and white and other high contrast checks, the cuttlefish camouflage pattern depended on the size of the checks. Disruptive patterns were employed when the check was between 40% and 120% of the area of the animals white square component. When the pattern was altered to a lower contrast (e.g. shades of grey) however, the camouflage pattern was independent of the check size, and was of the uniform/stippled pattern. At intermediary contrast levels the mottled pattern is seen with small area checks.

Evaluating background pattern contrast as well as check size as cue for uniform, mottled or disruptive camouflage pattern employment by S. officinalis
From Barbosa et al. (2008)(b)


Even with all the headway the lab is making on camouflage patterns in cephalopods, there is still much for them to look at. Especially vexing right now is the issue of color. Cephalopods have excellent color matching capabilities, at least during the daytime, at night they still employ excellent pattern camouflage but the color is off, in hue if not in intensity (Hanlon et al. 2007). What researchers wonder about however is how they are able to "see" the colors that they are using in their camouflage. Cephalopod eyes are beautiful structures, able to see polarized light, but they only have one receptor for color information. Cephalopods are colorblind (Mäthger et al. 2006) and see only in a blue-green at 492nm. So how do they "see" the colors they are imitating, since they are able to imitate the colors around them?

Lydia Mäthger and others from the lab are examining just that. They have recently had a paper published from experiments in which they measured the spectral reflectance of S. officinalis and of several marine substrates which would evoke the three different main camouflage patterns. They found that the spectral signatures, while not a match, do correlate closely, suggesting that the color variations in substrate and animal skin can be very similar and this may let the cuttlefish effectively match color without color vision.

So, yeah, that was a very cool seminar. All the better for the brief conversation afterward at the post-seminar social. It was exciting for Johann as well, since he was able to ask several questions and get answers straight from the guy who wrote the book. Since we lingered so long, my family decided to get Thai for dinner from a new restaurant near the school. First two items up on the specials for the night?

#1 Fried cuttlefish with Chili sauce. (sorry DC!)
#2 Jumping Squid with Thai Basil and Chili

Oh, yeah... Cephalopodtastic!


UPDATE:Want to get a taste of the video Roger treated us to? Want to see the invisible octopus, two faced squid, disappearing cuttlefish and moving rock?

David Gallo presented some of Roger's work at a TED talk a few years ago and has 3 minutes of the cephalopod porn video with all the requisite "Ooohs" and "Aaaaahs" from the crowd at Monterey Bay. I'll embed the low res version for your immediate gratification, but a high res version is also available for big screen drooling viewing pleasures. The cephalopods come after 2 minutes of almost as (if not as,) cool, deep sea bioluminescence.



A Barbosa, L Litman, R Hanlon (2008). Changeable cuttlefish camouflage is influenced by horizontal and vertical aspects of the visual background Journal of Comparative Physiology A, 194 (4), 405-413 DOI: 10.1007/s00359-007-0311-1

A Barbosa, L Mäthger, K Buresch, J Kelly, C Chubb, C Chiao, R Hanlon (2008). Cuttlefish camouflage: The effects of substrate contrast and size in evoking uniform, mottle or disruptive body patterns Vision Research, 48 (10), 1242-1253 DOI: 10.1016/j.visres.2008.02.011

A Barbosa, L Mäthger, C Chubb, C Florio, C Chiao, R Hanlon (2007). Disruptive coloration in cuttlefish: a visual perception mechanism that regulates ontogenetic adjustment of skin patterning Journal of Experimental Biology, 210 (7), 1139-1147 DOI: 10.1242/jeb.02741

R Hanlon, M Naud, J Forsythe, K Hall, A Watson, J McKechnie (2007). Adaptable Night Camouflage by Cuttlefish. The American Naturalist, 169 (4), 543-551 DOI: 10.1086/512106

R Hanlon, M Naud, P Shaw, J Havenhand (2005). Behavioural ecology: Transient sexual mimicry leads to fertilization Nature, 433 (7023), 212-212 DOI: 10.1038/433212a (Open Access)

L Mäthger, C Chiao, A Barbosa, R Hanlon (2008). Color matching on natural substrates in cuttlefish, Sepia officinalis Journal of Comparative Physiology A, 194 (6), 577-585 DOI: 10.1007/s00359-008-0332-4

L Mäthger, A Barbosa, S Miner, R Hanlon (2006). Color blindness and contrast perception in cuttlefish (Sepia officinalis) determined by a visual sensorimotor assay Vision Research, 46 (11), 1746-1753 DOI: 10.1016/j.visres.2005.09.035

R Sutherland, L Mäthger, R Hanlon, A Urbas, M Stone (2008). Cephalopod coloration model. II. Multiple layer skin effects Journal of the Optical Society of America A, 25 (8) DOI: 10.1364/JOSAA.25.002044 (Open Access)

2 comments:

  1. Eric, One of, possibly the, best posts from you yet! Certainly one of the most detailed. Well done!

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  2. Very nice indeed! I blogged about this research when it was in the NY Times, but this is so much cooler than the Times story!

    It’s good to see a thoughtful story,
    Showing us in all our glory!
    A walking (swimming) work of art,
    The skin we wear is really smart!
    Chameleons can only wish
    To emulate the cuttlefish;
    A master of the craft indeed,
    With changing hues at lightning speed,
    Resulting in a really slick
    Near-magic disappearing trick!
    Now Dr. Hanlon can surmise
    A simple trick to our disguise:
    Instead of thousands, only three
    Designs account for what you see,
    To help us disappear from view;
    The doctor says here’s what we do:
    We keep our color uniform,
    When solid backgrounds are the norm;
    If busy patterns come, we will
    Turn mottled—that will fill the bill;
    Our outlines disappear from sight
    With our disruptive dark and light.
    Discovering this rule of threes
    Is one of many mysteries;
    But many more are still unknown
    To those who lack a cuttlebone.

    http://digitalcuttlefish.blogspot.com/2008/02/stop-presses.html

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