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Science
Volume 40 Issue 14 • August 5-11, 2010
now in our 40th season

Playing Possum

by Dr. Sarah D. Oktay
Managing Director UMass Boston Nantucket Field Station

What’s white and looks like a dead whale floating on the water? Give up? I’ll give you a clue; the Discovery Channel’s famous Shark Week programming started August 1st.  My friend, Pete Kaizer, who is captain of the Nantucket-based sportfishing charter boat the “Althea K” (www.altheaksportfishing.com) discovered the answer to this riddle when he saw a huge white object floating in the water in late July and assumed that it was a dead whale.  Dead whale carcasses can be seen floating around Nantucket far offshore providing an oasis of food for birds, fish, and parasites. But this was no dead whale.  When Pete nudged the Althea K closer he could tell it was a Great White shark hanging belly up in the water with its tail and head arching downward. Pictures taken by Pete can be found at www.Yackon.com under the topic “Snoozing Great White.”  This shark was huge, almost 4 feet across at the pectoral fins and close to 15 feet long. It looked dead, but it wasn’t.  The shark was lying perpendicular to the ship, eerily motionless.  Pete thought they should pull up the head to see if it had been harpooned or shot or some other mishap had occurred so that they could call it in to the Coast Guard if needed.  Pete’s first mate, Dan Gault, wisely thought, “Before we try to roll it over or lift the head, let’s make sure it is dead,” so they poked it in the stomach with a long gaff.  Well, you can guess what happened next; the shark “woke up,” thrashed about, scared the bejesus out of everyone, then rolled over and made a byline for the deep.  As Pete poetically worded it, “it disappeared into the abyss” before they had scarcely realized what happened.
What he and his crew and passengers were witnessing was a classic case of the Great White exhibiting “tonic immobility” which is an antipredator adaptation or defense mechanism used by all types of creatures to protect themselves.  Animals such as sharks, beetles, snakes, and the opossum (possum), are capable of appearing to be dead to an observer, while otherwise alive.  (Some of my relatives might also be capable of this; especially when it comes to house cleaning). 

This could either be a reflex action, as in tonic immobility, or a defense mechanism for avoiding predators, as in thanatosis, which is probably adaptive, or "playing possum," which is more instinctive.

Tonic immobility is a natural state of paralysis that animals enter, in most cases when presented with a threat.  Scientists believe it is also used by some species to avoid mating (“not tonight dear, I’m dead”) and by others to encourage mating (see how spiders use this tactic below).  The term that best fits the situation is mainly dependant on whether the act is instinctual or inadvertent or deliberate.  Many mammals including possums that play dead are doing it deliberately.  But for a shark, the response is most likely unavoidable and an adaptive behavior to avoid a fight or sex, but not necessarily under the control of the shark.  One of the reasons why it is thought that sharks are exhibiting true tonic immobility is the fact that they normally need to keep swimming to move oxygen across their gills.

Unlike bony fish, sharks do not have gas-filled swim bladders for buoyancy.  Instead, sharks rely on a very large liver that is filled with oil containing squalene that provides buoyancy and the fact that their cartilage skeleton is about half as dense as bone.  This site: http://www.seaworld.org/animal-info/info-books/sharks-&-rays/anatomy.htm does a great job of illustrating simple shark anatomy and explaining the many amazing ways that sharks have adapted to their environment; for instance, check out the stomach inversion trick, a perfect weight loss tactic...but I digress.  A shark's liver is relatively large, making up to 25% of its total body weight and takes up to 90% of the space inside its body cavity.  Squalene is a natural compound that all animals produce.  It is a hydrocarbon and in humans it assists in the synthesis of steroid hormones, cholesterol, and Vitamin D.  It has a low density and a specific gravity of 0.855, making it the optimal material to assist the shark in maintaining buoyancy, as it is lighter than water.  The liver's effectiveness is limited, so sharks employ dynamic lift to maintain depth, sinking when they stop swimming.  Sand tiger sharks gulp air at the surface and then store it in their stomachs, using it as a form of swim bladder.  Most sharks need to constantly swim in order to breathe and cannot sleep very long, if at all, without sinking.  However certain shark species, like the nurse shark, are capable of pumping water across their gills, allowing them to rest on the ocean bottom.

Some sharks, if turned upside down in the water or stroked on the nose, enter a natural state of tonic immobility.  Researchers use this condition to handle sharks “safely” in the wild, giving them the opportunity to measure them without causing harm (en.wikipedia.org/wiki/Tonic_immobility).  The shark remains in this state of paralysis for an average of fifteen minutes before it recovers.  When testing sharks under this "tonic" state, scientists will put a chemical plume in the water to wake the shark.  In fact, this behavior is studied by scientists and chemists in order to develop effective shark repellents (more at http://www.sharkdefense.com/Repellents/Tonic_Immobility/tonic_immobility.html).
Even with large species like tiger sharks which can be 3–4 meters (10 to 15 feet) in length, tonic immobility may be achieved by placing ones hands lightly on the sides of the animal's snout approximate to the general area surrounding its eyes.  Great White sharks have been shown to be not as responsive as other species whenever tonic immobility has been attempted ( I’m glad that is not my area of expertise, that would be a somewhat short lived experiment).  One of the reasons scientists believe that tonic immobility may be linked with defense is because female sharks seem more responsive than others.  Pete’s photos seem to show a female Great White, although it is a little tough to tell whether the male claspers are present.  During tonic immobility, the dorsal fins straighten, and both breathing and muscle contractions become more steady and relaxed.
In animal behavior, thanatosis (from Greek thanatos, “death,” and -osis, 'state of disease') is the process by which an animal feigns death in order to evade unwelcome attention, such as that of a predator, or a male trying to mate with a female.  In Greek mythology, Thánatos was the personification of Death.  The Greek poet Hesiod established in his Theogony that Thánatos is a son of Nyx (Night) and Erebos (Darkness) and twin of Hypnos (Sleep), which makes sense when you consider the state these creatures exhibit is similar to hypnosis.  The use of thanatosis assumes that the pursuer will give up on the chase and the kill and ignore the victim, as most predators only catch live prey.  For obvious reasons, it is usually employed only when escape is impossible.  Some scientists theorize thanatosis is a form of self-mimesis, a type of camouflage or mimicry in which the "mimic" imitates itself in a dead state, such that its pursuer no longer takes notice of it.  It is a phenomenon known in invertebrates such as wasps, beetles, fiddler crabs, and crickets, but also in vertebrates such as the common opossum, frogs, some lizards and snakes.  Artificial selection experiments have shown that there is heritable variation for length of death-feigning in beetles, and that those selected for longer death-feigning durations are at a selective advantage to those at shorter durations when a predator is introduced, which suggests that thanatosis is indeed adaptive.  If you do a search online, you will find many papers describing each animal that uses it.  Unfortunately; this behavior is not thought to do much for possums, who often end up as road kill because they employ this tactic.

The documentary The Whale That Ate Jaws shows one of the most incredible instances of an Orca, or Killer Whale, suffocating a Great White by turning it over and inducing tonic immobility until it drowned and could be eaten.  This happened in 1997, just off the Farallon Islands, when a group of whale watchers watched this Orca prey upon a great white shark that may have been a threat to younger members of the orca pod.  The ability to adapt their behavior into such a high risk defense mechanism is truly astounding.  Read more: http://channel.nationalgeographic.com/series/nature-untamed#tab-Videos/07503_00#ixzz0vRHppL51

Maybe not as exciting but certainly memorable if it has ever happened to you is thanatosis exhibited by snakes in the wild.  For instance, when a hog-nosed snake rolls onto its back and appears to be dead when threatened by a predator, a foul-smelling, volatile fluid oozes from its body.  Predators, such as cats, then lose interest in the snake, which both looks, and smells, dead. One reason for their loss of interest is that rotten smelling animals are avoided as a precaution against infectious disease, so this works as a very effective deterrent from predators.  I assume it would cut down on unwanted mating too.

Animals may also exhibit thanatosis in the boudoir. In the article published in Behavioral Ecology (authors Line Spinner Hansen, Sofia Fernandez Gonzales, Søren Toft and Trine Bildea, 2008 19(3):546-551) called “Thanatosis as an adaptive male mating strategy in the nuptial gift–giving spider Pisaura mirabilis,” you find that male members of the spider species Pisaura mirabilis, more reassuringly known as the nursery web spider, “display a spectacular mating behavior involving a nuptial gift and thanatosis (death feigning).  Thanatosis in a sexual context is exceptional and was suggested to function as an antipredation strategy toward potentially cannibalistic females.” In other words, by feigning death, the male spiders attracted more mates and more action overall and often lived to tell the tale.  If I haven’t completely scared you, check out some pictures of the nursery web spider including some males with missing legs who I guess did win the “playing dead” game at http://www.eurospiders.com/Pisaura_mirabilis.htm.

 

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