What do I have in common with great white sharks, black widow spiders, snakes and opossums? Thanatosis, or tonic immobility. What is this? Well most people know this phenomenon as ‘playing possum’. I first discovered that I shared this trait with some of the most fearsome of animals when I fell off the back of a truck and was catapulted down a hill. As soon as I felt my body begin to leave the back of the pick-up, I went limp and ‘blacked out’. I have no recollection about my trip down the hill, but observers remarked that it was spectacular. Everyone, including myself, was shocked when I ‘woke up’ to find that I had not broken a single bone, nor so much as sprained a joint. The only evidence of my journey was a minor scrape on one knee. A second incident further convinced me that I had a special knack for ‘playing possum’. I used to volunteer for an orangutan and chimpanzee sanctuary. One day, a young chimpanzee ran over to me and jumped in my lap, hugging me. A few seconds later, he was startled and screamed, reaching for my neck with his teeth. All it took was for me to hear him scream and I folded like a deck of cards. Literally. I went limp, ‘blacked out’, and woke up once he was off of me. Upon waking, I found that I had received a shallow bite to the neck, but was otherwise uninjured. It struck me that if I had struggled against him my injuries might have been more severe. On the other hand, I was concerned that my inability to remain active during a threat could be problematic. I worried that if I needed to act I would be unable to do so because I always seemed to pass out! A third and final incident resolved this concern for me. Several years ago I was in a near fatal car accident. I say near fatal because, but for my actions, I don’t think I would have survived. Upon impact I was thrust into a sea of trees. I distinctly remember steering the car to avoid the trees. I was successful only briefly and when I realized impact with a tree was inevitable, I placed my hands in my lap, put my head down, and you guessed it, ‘blacked out’. I walked (okay crawled) out of the car with no serious physical injuries, no whiplash, etc. So it would seem that when action is possible and likely to allow me to successfully avoid a threat, I act. When it is unavoidable, however, it seems my strategy is to remove myself from the situation, metaphorically speaking. This got me wondering what goes on in animals and if this trait is adaptive?
As I already mentioned, the official term for ‘playing possum’ is called thanatosis, which loosely translates to-apparent death. I suppose it got its nickname because 1) it is much more entertaining to say ‘playing possum’ than thanatosis and 2) because people are more likely to see an opossum do it, than say, a shark. But I am only speculating. Why do animals feign death? A number of ideas have been suggested including:
1. predators don’t like to eat already dead prey (generally)
2. it is a form of physical defense (though obviously passive) from predators, from mates that are harassing you, and even from hostile members of your own species
3. you can blend in better with the background if you play dead
4. since most predators like to chase their food, if you don’t move, there is no chase
5. prey that play dead may indicate that they are dangerous to eat and will taste bad
Let’s talk about spiders first. There have been movies made about them, drawing parallels to humans, specifically warning men of the dangers associated with ‘black widows’, or women that kill their husbands. Sexual cannibalism will probably be a separate topic altogether, but it is relevant here because males in some spider species have come up with a way to avoid being eaten by their love interest. They play dead. In many species the male presents the female with a gift. This gift is referred to as a ‘nuptial’ gift and usually consists of food. Maybe he is hoping that if he gives her enough food, she will forgo eating him as her meal! That may not work for many species though, since females will eat the male before he has a chance to mate with her. It is as if she decides he’s good enough to eat but not good enough to mate with! To deal with this mating dilemma, males will enter thanatosis. In the nursery web spider, the males have an elaborate strategy. First the male raises his body to nearly vertical and presents the female with a nuptial gift and conveniently ‘hides’ his abdomen (body) behind this gift to protect himself. When the female approaches, sometimes she goes for the gift. Sometimes, however, she bypasses the gift and goes for the male. It is at this exact moment that the male enters a motionless state. He does this by still holding the gift in his chelicerae, usually the two mouthparts found in the front, while extending his legs backwards, stretched out and completely motionless. The female can go so far as to grab onto the gift and drag it and the male along. If, however, the female begins to consume the gift, the male ‘magically’ pops back to life and initiates copulation while she is otherwise…ahem…occupied. Don’t think he relaxes for one second, though. The male, ever cautious, usually maintains contact with one leg on the nuptial gift possibly to keep track of what the female is up to. This strategy seems to work in the male’s favor as all males that ‘played dead’ were able to mate. For the ones that didn’t, well you can just imagine their fate!
In black-widow spiders, considered the most venomous of all spiders, thanatosis, or tonic immobility, is used for protection, even by the females who have much larger venom sacks than males. A small preliminary study reported that by tapping females on the back firmly with the hard end of a paintbrush, black widows will feign death. So why play possum when you have the means to attack back? One thought is that it may be costly to fight back. You have to use energy, or in the case of black widow, venom, which is energetically costly to produce. Depending on the threat, it may be more advantageous to conserve your energy and wait it out. This strategy works well if the particular predator in question only likes to eat live prey.
Venomous spiders are not alone in this behavior. Snakes do this too. When threatened, many species will play dead. This may not be their first tactic though. The hog-nosed snake for instance may rear up, looking very similar to a cobra. If all else fails, however, it will flop over onto its back with its mouth open and its tongue drooping out of its mouth and then it will release a foul smelling fluid in an attempt to convince the predator that it is dead, rotting, and will not appeal to the predator’s palate.
An interesting question then is: do top predators ever ‘play possum’? Yes they do. In the group that includes sharks, rays and skates, (Elasmobranchs) it manifests itself with the individual usually inverted. For this group of species, once immobility occurs it can last anywhere from under a minute to several hours. The list of sharks that display this behavior continues to grow and includes several species of dogfish shark, the lemon shark, the sandbar shark, the swellshark, the leopard shark, the blacktip reef shark, the whitetip reef shark, and the Caribbean reef shark. How exactly can we determine whether or not a shark feigns death? If you guessed that it somehow involves handling the shark and turning it upside down, you would be correct. Don’t you want to be part of that research team? Basically the shark is caught and then gently, but quickly inverted. Apparently sharks find this threatening and will go limp. You think?
Okay, but what about the mightiest of sharks, the top of the food chain, the most feared creature in the ocean (unnecessarily, I might add): the Great White? Yes, even they will exhibit this behavior. It was briefly seen on a National Geographic special “The Whale That Ate Jaws". This technique, though used by the shark to protect itself, could prove deadly. Why? Because some sharks, including great whites and hammerheads, need to keep moving to breath. If they remained in the hypnotic state too long, they would simply suffocate. There are some shark enthusiasts who seem to enjoy inducing this in wild sharks and not only is this a bad idea, but they fail to understand that this response is an extreme stress/trauma response. There is no excuse for any person to deliberately traumatize an animal for the entertainment of themselves or others.
What these examples reveal is that, for many species, tonic immobility is an extreme reaction to a life threatening and fearful situation. Not only that, but for some it is employed only when all other defense reactions fail. I can see now, how in the context of my experiences, this is true. In the first two incidences, there was no opportunity for any other reaction. In the accident, it was only after all else failed that I entered this state. This response has been found in all taxa, including humans, except jawless fish. In humans, like in other animals, it is not a learned response that one can develop. Meaning, it is an automatic response, not a coping strategy. Perhaps I am not such an outlier after all.
References:
Bilde, T et al. 2006. Death feigning in the face of sexual cannibalism Biology Letters, 2:23–25.
Cassill, D. L., Vo, K. & Becker, B. 2008 Young fire ant workers feign death and survive aggressive neighbors. Naturwissenschaften 95, 617–624.
Miyatake, T., Katayama, K., Takeda, Y., Nakashima, A., Sugita, A. & Mizumoto, M. 2004 Is death-feigning adaptive? Heritable variation in fitness difference of death-feigning behaviour. Proc. R. Soc. Lond. B 271, 2293–2296.
Tuesday, October 26, 2010
Friday, October 8, 2010
Keeping Track of Time: It’s All Relative
A few weeks ago NPR’s All Things Considered did a story on recent research supporting Einstein’s Theory of Relativity (see Full Story). Einstein posited that time is affected by your position relative to a gravitational field and by how fast you are moving through space. Dr. Chin-Wen Chou and colleagues demonstrated the validity of Einstein’s theory using atomic clocks placed at different heights. The clock placed a mere 33 centimeters above the other ticked at a faster pace than the one below. Of course, the time difference was infinitesimally small, but different nonetheless. This research got me wondering that since time is relative, not only literally but perceptually as well (hadn’t you noticed), how do animals perceive time? More interesting perhaps, do they perceive time at all?
It seems that my random thoughts led me to stumble across a contentious issue, one almost as controversial as language. A member of the Brambell Committee, Bill Thorpe, raised the question about whether or not animals live solely in the present moment in the 1960’s. He argued that few animals remember the past, even fewer can fear the future, but that animal welfare regulations should account for the capacity of some animals to suffer in their own mind. In general, this ability to mentally time travel has been, like language, argued to be an expressly human trait. To further this argument, researchers have suggested that language itself allows for mental time travel. This makes a nice circular line of reasoning that no animal can penetrate. If animals do not have language, then they cannot time travel. If they only feel pain in the moment and are not traumatized by their memory of that pain or the anticipation of future pain, this provides a neat excuse for human behavior towards animals. However, science often moves forward through dissent and many researchers have challenged the conclusion that animals are “stuck in time”. The result is decades of research that is beginning to provide new insights into the capacity of animals to remember and anticipate the future.
The primary type of memory dealing with time is episodic memory and there are several definitions. A classic definition incorporates: what happened, where did it happen, and when did it happen. Keep in mind that the focus is on unique events or episodes. Because we can ask people about their episodic memory using a common language, it is clear that humans have episodic memory. When dealing with non-verbal animals this becomes a bit tricky and behavioral criteria replace verbal responses. In the examples below episodic memory in animals is frequently referred to semantically as “episodic-like” due to the inability to verbally confirm the temporal nature of the memory, but functionally it is the same.
Scrub jays have led the way on revealing the potential for animals to remember and have a working concept of time. Scrub jays are members of the Corvid family. Smaller than the closely related blue jay, scrub jays are frequently found in open habitats dominated by oak woodlands, chaparral, or pinyon-juniper woodlands. The Western scrub jay has long been a model species for studying food caching behavior, spatial memory, and cognitive behavior. Scrub jays store, or cache, their food in many different locations. Usually if you have to store your food it seems like a good idea to remember where you put it. Therefore you can predict that animals that store their food in different locations will, at the very least, have superb spatial memory. Unlike many humans who find that locating their car keys can present unique challenges. If you store your food and that food can spoil, it seems obvious that it would be beneficial to also remember what you stored when. Indeed, several clever experiments have revealed that these remarkable birds learn to avoid recovering food when a long time has gone by and the food has become inedible. Using two types of food sources and allowing the birds to recover stored food at different time intervals, the birds recovered their preferred food item (worms-yummy!) at the shortest time interval when the worms were still fresh and then switched to recovering the other food source (peanuts) at the longer time interval when the worms were decayed. Controls were used to eliminate the use of sight and smell for food recovery, demonstrating that the birds remembered what was stored where and, more importantly, when the items were stored.
The humble lab mouse also has episodic-like memory. Like the scrub jay, experiments have been used to test whether mice remember what item was stored, where it was stored, and in what order. Results show that mice recognize objects they have previously encountered, they remember where they came across these particular objects, and even discriminate the temporal order in which they were presented with different objects. So how exactly does one determine the time component here? Mice were presented with two different objects made of plastic and precautions were undertaken to ensure that odor cues could not be used to distinguish between the two objects and that the mice didn’t have a wacky preference for one or the other of the objects. The mice were placed in an open field with a set of four of one of the objects placed in each corner of the field in random order. After 50 minutes, four copies of the second object were placed in each of the corners. After another 50 minutes, the process was repeated but this time 2 copies of the object used the first time (100 minutes prior) and 2 copies of the “recent” object (50 minutes prior) were places in the corners. Spatial configurations of where the old and new objects were placed tested for the what/where component. Basically, the mice spent more time checking out the “old” objects. Similar experiments with rats have yielded the same result, indicating that there is a clear concept of what, where and when a novel item was encountered. By the way, the 50-minute interval in the mice experiments was chosen based on the time interval used for rats (65 minutes). Though not clear, the values of 100 minutes ago and 130 minutes ago, respectively, may represent the upper limit of time perception in these species. However, it may be more likely that we just have to get more creative in our experiments to assess how long ago they can remember.
Let’s hop back to birds for a moment and talk about the black-capped chickadee. I became fond of these little birds during my time on Long Island. There was little that I enjoyed about living there, but visiting a park where these little birds courageously landed on your hand to gently pluck a sunflower seed out of your palm always made me smile. Somehow I felt like singing a Snow White song and skipping merrily down the path. Like the scrub jays discussed above, black-capped chickadees store food. Therefore, we can already predict that it may be very important to their survival to remember what they store where and how long ago. Similar to the scrub jay experiments, birds visited sites at short intervals (3 hours) or long intervals (123 hours) selecting the food source at short intervals that would not yet be spoiled (mealworms) and visiting the sites that had sunflowers at the longer time interval. Since many birds store their food for access over the winter it is likely that their memory would extend beyond the 123 hours in the experiment. On side note, a second experiment of foraging in an aviary showed that chickadees remember when even if the task at hand does not involve storage and retrieval.
If birds, bees, humming birds, and rodents can do it, then surely apes can too, right? We’re still talking about remembering when…
A study on three species of great ape (bonobo, chimpanzee, orangutan) using food retrieval showed that all three integrated the what, where and how long ago components of the task. What was interesting though was that bonobos and chimpanzees individuals younger than seven and older than 18 were a bit slower on the time component. This is particularly striking because episodic memory in humans shows the same age-dependent pattern (though the specific ages vary). This may indicate similarities in the development of information encoding and storage processes. Not to be excluded, similar findings were reported for a male gorilla named King.
Thus far the discussion has only considered remembering the ‘past’. An intriguing question is can animals anticipate the future? The research on this aspect of mental time travel is under-explored, but once again, this is primarily due to the difficulties associated with identifying what indicates future planning in non-verbal species. However, some research has been done on scrub jays, chimpanzees, and orangutans that does support the existence of future thought by animals. There are several implications of this research, not the least of which directly involves the regulations surrounding animal welfare. Now that is food for future thought...
References:
Chou,C.W., Hume, D.B., Rosenband, T., and Wineland, D.J. 2010. Optical clocks and relativity. Science 329: 1630-1633.
Clayton, N.S. and Dickinson, A. 1998. Episodic-like memory during cache recovery by scrub jays. Nature, 395: 272-274.
Clayton N.S., Bussey, T.J., and Dickinson, A. 2003. Can animals recall the
past and plan for the future? Nat Rev Neuroscience 4:685–691.
Dere, E., Huston, J.P., and De Souza Silva, M.A. 2005. Episodic-like memory in mice: Simultaneous assessment of object, place and temporal order memory. Brain Research Protocols, 16:10-19.
Feeney, M.C., Roberts, W.A., and Sherry, D.F. 2009. Memory for what, where, and when in the black-capped chickadee (Poecile atricapillus). Animal Cognition, 12:767-777.
Henderson J, Hurly TA, Bateson M, Healy SD (2006) Timing in free
living rufous humming birds, Selasphorus rufus. Current Biology,16:512–515
Lea, S.E.G., 2001. Anticipation and memory as criteria for special welfare consideration. Animal Welfare, 10:S195–S208.
Martin-Ordas, G. Haun, D., Colmenares, F., and Call, J. 2010. Keeping track of time: evidence for episodic-like memory in great apes. Animal Cognition, 13:331-340.
Osvath M, Osvath H (2008) Chimpanzee (Pan troglodytes) and
orangutan (Pongo abelii) forethought: self-control and pre-experience in the face of future tool use. Animal Cognition, 11:661–674.
Schwartz, B.L., HoVman, M.L., and Evans, S. 2006. Episodic-like memory in a gorilla: A review and new findings. Learning and Motivation, 36:226-244.
Tulving, E. 1972. Episodic and semantic memory. In: Tulving E, Donaldson, W (eds) Organization of memory. Academic, San Diego, pp 381–403.
Tulving, E. 1983. Elements of episodic memory. Clarendon Press, Oxford
It seems that my random thoughts led me to stumble across a contentious issue, one almost as controversial as language. A member of the Brambell Committee, Bill Thorpe, raised the question about whether or not animals live solely in the present moment in the 1960’s. He argued that few animals remember the past, even fewer can fear the future, but that animal welfare regulations should account for the capacity of some animals to suffer in their own mind. In general, this ability to mentally time travel has been, like language, argued to be an expressly human trait. To further this argument, researchers have suggested that language itself allows for mental time travel. This makes a nice circular line of reasoning that no animal can penetrate. If animals do not have language, then they cannot time travel. If they only feel pain in the moment and are not traumatized by their memory of that pain or the anticipation of future pain, this provides a neat excuse for human behavior towards animals. However, science often moves forward through dissent and many researchers have challenged the conclusion that animals are “stuck in time”. The result is decades of research that is beginning to provide new insights into the capacity of animals to remember and anticipate the future.
The primary type of memory dealing with time is episodic memory and there are several definitions. A classic definition incorporates: what happened, where did it happen, and when did it happen. Keep in mind that the focus is on unique events or episodes. Because we can ask people about their episodic memory using a common language, it is clear that humans have episodic memory. When dealing with non-verbal animals this becomes a bit tricky and behavioral criteria replace verbal responses. In the examples below episodic memory in animals is frequently referred to semantically as “episodic-like” due to the inability to verbally confirm the temporal nature of the memory, but functionally it is the same.
Scrub jays have led the way on revealing the potential for animals to remember and have a working concept of time. Scrub jays are members of the Corvid family. Smaller than the closely related blue jay, scrub jays are frequently found in open habitats dominated by oak woodlands, chaparral, or pinyon-juniper woodlands. The Western scrub jay has long been a model species for studying food caching behavior, spatial memory, and cognitive behavior. Scrub jays store, or cache, their food in many different locations. Usually if you have to store your food it seems like a good idea to remember where you put it. Therefore you can predict that animals that store their food in different locations will, at the very least, have superb spatial memory. Unlike many humans who find that locating their car keys can present unique challenges. If you store your food and that food can spoil, it seems obvious that it would be beneficial to also remember what you stored when. Indeed, several clever experiments have revealed that these remarkable birds learn to avoid recovering food when a long time has gone by and the food has become inedible. Using two types of food sources and allowing the birds to recover stored food at different time intervals, the birds recovered their preferred food item (worms-yummy!) at the shortest time interval when the worms were still fresh and then switched to recovering the other food source (peanuts) at the longer time interval when the worms were decayed. Controls were used to eliminate the use of sight and smell for food recovery, demonstrating that the birds remembered what was stored where and, more importantly, when the items were stored.
The humble lab mouse also has episodic-like memory. Like the scrub jay, experiments have been used to test whether mice remember what item was stored, where it was stored, and in what order. Results show that mice recognize objects they have previously encountered, they remember where they came across these particular objects, and even discriminate the temporal order in which they were presented with different objects. So how exactly does one determine the time component here? Mice were presented with two different objects made of plastic and precautions were undertaken to ensure that odor cues could not be used to distinguish between the two objects and that the mice didn’t have a wacky preference for one or the other of the objects. The mice were placed in an open field with a set of four of one of the objects placed in each corner of the field in random order. After 50 minutes, four copies of the second object were placed in each of the corners. After another 50 minutes, the process was repeated but this time 2 copies of the object used the first time (100 minutes prior) and 2 copies of the “recent” object (50 minutes prior) were places in the corners. Spatial configurations of where the old and new objects were placed tested for the what/where component. Basically, the mice spent more time checking out the “old” objects. Similar experiments with rats have yielded the same result, indicating that there is a clear concept of what, where and when a novel item was encountered. By the way, the 50-minute interval in the mice experiments was chosen based on the time interval used for rats (65 minutes). Though not clear, the values of 100 minutes ago and 130 minutes ago, respectively, may represent the upper limit of time perception in these species. However, it may be more likely that we just have to get more creative in our experiments to assess how long ago they can remember.
Let’s hop back to birds for a moment and talk about the black-capped chickadee. I became fond of these little birds during my time on Long Island. There was little that I enjoyed about living there, but visiting a park where these little birds courageously landed on your hand to gently pluck a sunflower seed out of your palm always made me smile. Somehow I felt like singing a Snow White song and skipping merrily down the path. Like the scrub jays discussed above, black-capped chickadees store food. Therefore, we can already predict that it may be very important to their survival to remember what they store where and how long ago. Similar to the scrub jay experiments, birds visited sites at short intervals (3 hours) or long intervals (123 hours) selecting the food source at short intervals that would not yet be spoiled (mealworms) and visiting the sites that had sunflowers at the longer time interval. Since many birds store their food for access over the winter it is likely that their memory would extend beyond the 123 hours in the experiment. On side note, a second experiment of foraging in an aviary showed that chickadees remember when even if the task at hand does not involve storage and retrieval.
If birds, bees, humming birds, and rodents can do it, then surely apes can too, right? We’re still talking about remembering when…
A study on three species of great ape (bonobo, chimpanzee, orangutan) using food retrieval showed that all three integrated the what, where and how long ago components of the task. What was interesting though was that bonobos and chimpanzees individuals younger than seven and older than 18 were a bit slower on the time component. This is particularly striking because episodic memory in humans shows the same age-dependent pattern (though the specific ages vary). This may indicate similarities in the development of information encoding and storage processes. Not to be excluded, similar findings were reported for a male gorilla named King.
Thus far the discussion has only considered remembering the ‘past’. An intriguing question is can animals anticipate the future? The research on this aspect of mental time travel is under-explored, but once again, this is primarily due to the difficulties associated with identifying what indicates future planning in non-verbal species. However, some research has been done on scrub jays, chimpanzees, and orangutans that does support the existence of future thought by animals. There are several implications of this research, not the least of which directly involves the regulations surrounding animal welfare. Now that is food for future thought...
References:
Chou,C.W., Hume, D.B., Rosenband, T., and Wineland, D.J. 2010. Optical clocks and relativity. Science 329: 1630-1633.
Clayton, N.S. and Dickinson, A. 1998. Episodic-like memory during cache recovery by scrub jays. Nature, 395: 272-274.
Clayton N.S., Bussey, T.J., and Dickinson, A. 2003. Can animals recall the
past and plan for the future? Nat Rev Neuroscience 4:685–691.
Dere, E., Huston, J.P., and De Souza Silva, M.A. 2005. Episodic-like memory in mice: Simultaneous assessment of object, place and temporal order memory. Brain Research Protocols, 16:10-19.
Feeney, M.C., Roberts, W.A., and Sherry, D.F. 2009. Memory for what, where, and when in the black-capped chickadee (Poecile atricapillus). Animal Cognition, 12:767-777.
Henderson J, Hurly TA, Bateson M, Healy SD (2006) Timing in free
living rufous humming birds, Selasphorus rufus. Current Biology,16:512–515
Lea, S.E.G., 2001. Anticipation and memory as criteria for special welfare consideration. Animal Welfare, 10:S195–S208.
Martin-Ordas, G. Haun, D., Colmenares, F., and Call, J. 2010. Keeping track of time: evidence for episodic-like memory in great apes. Animal Cognition, 13:331-340.
Osvath M, Osvath H (2008) Chimpanzee (Pan troglodytes) and
orangutan (Pongo abelii) forethought: self-control and pre-experience in the face of future tool use. Animal Cognition, 11:661–674.
Schwartz, B.L., HoVman, M.L., and Evans, S. 2006. Episodic-like memory in a gorilla: A review and new findings. Learning and Motivation, 36:226-244.
Tulving, E. 1972. Episodic and semantic memory. In: Tulving E, Donaldson, W (eds) Organization of memory. Academic, San Diego, pp 381–403.
Tulving, E. 1983. Elements of episodic memory. Clarendon Press, Oxford
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