Thursday, January 23, 2014

Houdini Skin: Now You Sea It, Now You Don't!

 Aubrie Fowler

ALL ABOARD THE MAGIC SCHOOL BUS!! It’s time for this bus to transform into a submarine!
Today we are delving deep into the tissues of some intelligent sea creatures in the group Cephalopoda (“head-feet”). As you may have seen (and if not, you’re going to be amazed by this fantastic footage), some cephalopods, including octopuses (check out this other BIO 502 blog post if you are not convinced my grammar is correct) and cuttlefish, change not only their coloration but also their texture. They can make their skin change from smooth and flat to rugose and 3-D to blend in with their surroundings. This is a unique behavior that has tickled my curiosity for years.
Some of the appearance changes, e.g. pigment, are for signaling and communication with other members of the same species or as a warning to other species. However, texture is primarily a means of camouflage, or blending in with the environment to escape predation. They use their excellent vision which is afforded by their powerful compound eyes: they use polarization to visually detect objects, such as their prey or a predator. These cues are turned into nerve impulses that are sent to effector muscles to alter texture, color, contrast, locomotion, and body posture.
The "flamboyant" cuttlefish (above) indicates that it is poisonous with its vibrant, showy display.
At the drop of a hat, octopus and cuttlefish can transform their skin to resemble kelp or spiky rocks in their environment. So how do they do it?
The change in texture is made possible by structures called skin papillae, which are small nipple-like projections of tissue that function as muscular hydrostats (water pressure that is exerted or transmitted). Papillae are made of dermal erector muscles (dem) that provide movement and structural support in the absence of rigid supporting elements such as cartilage or bone. Specifically, circular dem at the papilla base contract and push the tissue up to give the projections of skin height whereas horizontally arranged dermal erector muscles determine the shape, similar to a tent with elastic tent poles made of connective tissue. Muscular hydrostats like these are also found in cephalopod arms, tentacles, and suckers, vertebrate tongues, and even elephant trunks!

Here is a schematic illustrating the small dorsal papilla and the functional morphology: blood vessel (bv), light purple; chromatophore pigment cells (ch), brown or yellow; connective tissue, blue; dermal erector muscle (dem), medium pink; epidermis (ep), light pink; muscular core (mc), medium pink; nerve (n), very light purple; structural reflectors (ref); iridophores (ir), dark pink; leucophores (leu), dark blue; subepidermal muscle (sem), medium pink.

Now that we have addressed the texture change, what about the color? In the animal kingdom, there are many other species that can change color (notably on various timescales) such as chameleons, frogs, hares, flounder, and seahorses. Specifically in cuttlefish, on each papilla there are structural reflectors that reflect light like small mirrors called leucophores and iridophores. Leucophores are elongated, flattened cells covered in tiny, stalked 'knobs' (light bulb shaped) called the leucosomes that scatter light to reflect white light. Iridophores have multi-layer stacks of thin chitin, a type of carbohydrate, plates alternating with layers of cytoplasm that reflect a quarter of the wavelength absorbed to transmit colorless light). Aside from the iridescent reflection from these cells, there are also pigmented chromatophores.
The chromatophores of cephalopods are different from those of other animals because they are not controlled hormonally and are neuromuscular organs rather than cells. A chromatophore is an elastic pigment-containg sack attached to muscles, nerves, and glia. When excited the muscles contract, the chromatophore expands; when muscles relax, the chromatophore shrinks.

Chromatophores can expose or hide structural reflectors to control what the papilla looks like to other animals. Additionally, communication via body patterns is also conserved in many species throughout the generations. Moreover, the size and density of chromatophores depends greatly upon lifestyle and diet of that particular organism. For instance, a deep sea octopus that hides in rocky crevices likely has a different coloration than an octopus that resides amongst corals in the sandy shallows.

What is really miraculous about the skin is not just that the texture and color changes, but also that the cells coordinate. My fascination with this was sparked by the chromatophore music video. To coordinate, the network of subepidermal muscles retracts papillae as well as generates lateral movements along the surface of the mantle or body. This contraction and shortening flattens adjacent papilla for a coordination of bumpy and smooth skin, much like the appearance of a windblown sea. Thus far, more details of how the brain and nervous system control this coordination is largely unknown. 

Case Study: The Blue-ringed Octopus
A particularly fascinating example of color change is in the Blue-ringed octopus that uses its blue rings to serve as a “back off buddy, I’m toxic!” warning for predators. The Blue-ringed octopus is highly toxic due to a chemical called tetrodotoxin (TTX), which binds to voltage-gated sodium channels to block sodium ion movement into the cell so no action potential is generated, thereby halting nervous system activity.
WOAH! This school field trip is getting a little dangerous! Better make sure to listen to the teacher so we don’t get attacked by the octopus!!
While it is still unknown whether TTX, is produced by symbiotic bacteria or the octopus itself, it has been shown that the Blue-ringed octopus has a unique mechanism to quickly and conspicuously flash about 60 iridescent rings (and possibly even bite with enough toxins to kill a human!).
The rings have multiple layers of physiologically inert reflectors that reflect blue–green light. Surprisingly, there is an absence of chromatophores above the ring whereas most cephalopod chromatophores are used to partially cover or alter iridescence. Direct neural control is used to control muscles to make fast flashes on the rings by contracting and relaxing to expose or hide iridescence. In all, this method of hiding structural reflectors, which reflect shorter wavelengths that are not easily absorbed by water, is a creative way to continue to flash blue-green while still being able to use the rest of the body’s chromatophores for camouflage patterns.  The common octopus (Octopus vulgaris) takes an entire two seconds to show a full threat display. In contrast, the Blue-ringed octopus has a much quicker warning display, likely an evolutionary advantage because producing toxin is costly (as is getting eaten for both the predator and prey!).
We’re coming back up to the water's surface! I’m so happy to have my flippers feet on dry land again! Miss. Frizzle said our next adventure will take us into the human eye...time to prepare for another wild ride in science!
To learn more about camouflage in Cephalopods, I highly recommend watching the video that inspired me to write this blog, NOVA’s episode entitled “Kings of Camouflage”. 

Works Cited

Allen, J.J., G.R.R. Bell, A.M. Kuzirian, and R.T. Hanlon. 2013. Cuttlefish skin papilla morphology suggests a muscular hydrostatic function for rapid changeability. Journal of Morphology 274:645-656. 

Cartron, L., N. Josef, A. Lerner, S. McCusker, A. Darmaillacq, L. Dickel, and N. Shashar. 2013. Polarization vision can improve object detection in turbid waters by cuttlefish.  Journal of Experimental Marine Biology and Ecology 447:80-85.
Hanlon, R. T. 2007. Cephalopod dynamic camouflage. Current Biology 17:R400-R404.
Lee, C.H. and P.C. Ruben. 2008. Interaction between voltage-gated sodium channels and the neurotoxin, tetrodotoxin. Channels 2:407-412.
Mäthger, L.M., G.R.R. Bell, A.M. Kuzirian, J.J. Allen, and R.T. Hanlon. 2012. How does the Blue-ringed Octopus (Hapalochlaena lunulata) flash its blue rings? Journal of Experimental Biology 215:3752-3757. 
Messenger, J.B. 2001. Cephalopod chromatophores: neurobiology and natural history. Biology Reviews 76:473-528.

Williams, B.L., C.T. Hanifin, E.D. Brodie, Jr., and R.L. Caldwell. 2011. Ontogeny of tetrodotoxin levels in Blue-ringed Octopuses: Maternal investment and apparent independent production in offspring of Hapalochlaena lunulata. Journal of Chemical Ecology 37:10–17. 

Images & Videos









  1. Great use of videos and visuals. I couldn't believe it when I saw that first example of camouflage.

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