Back to the Future – Mental Time Travel in Tropical Birds?

I may not have a nuclear-powered DeLorean parked in my driveway, but I can travel in my own personal time machine anytime I want, and so can you.

Through what’s known as mental time travel, or MTT, you can move backwards and forwards through time – visiting the past when you remember a specific event you’ve already experienced, and then zipping forward to the future as you use this memory to predict, plan for and shape events that are yet to come.

Mental time travel is no mean feat: it implicates sophisticated cognitive processes and is thought to form the foundation for advanced forms of consciousness such as self-awareness and the ability to attribute independent thought, desires and intentions to others (an ability sometimes referred to as “theory of mind”).

So, can other animals engage in mental time travel? Perhaps not surprisingly, this has been a controversial topic, and many have argued that we humans are the only ones able to mentally flit about the fourth dimension, leaving all other animals stuck in the here and now. Although this may be partly attributable to our anthropocentric world view1, the language barrier between humans and other animals also poses a real problem, as it’s difficult to design MTT experiments that don’t involve interviews, since the best time travel evidence may consist of the voyager’s personal and subjective reports of the experience. Accordingly, solid evidence for MTT in other animals has been limited, and much of the evidence that does exist consists of anecdotal accounts and a small number of experiments involving great apes and western scrub-jays.

In a paper2 published in the October 14, 2011, issue of Behavioral Ecology, though, a research team led by Corina Logan of the Department of Experimental Psychology at the University of Cambridge proposed an intriguing new avenue for further research, one that might significantly expand the number of species that may be tested for MTT abilities. More specifically, Logan and her colleagues identified a specialized strategy among birds – army ant bivouac checking – that may provide conditions in the wild that could favor the development of mental time travel in a variety of species.

If I go back in time and shoot my grandmother, does that mean I’ll never be born?? (White Whiskered Puffbird, credit Glenn M. Duggan FZS)

While many tropical rain forest birds earn an opportunistic living by gobbling up insects and other small invertebrates flushed out of hiding by army ants on food raids, a subset go a step further – after raids by a specific army ant species (Eciton burchellii), these birds follow the ants back to their temporary nests (known as a bivouacs) in the evening, and then return to check on the bivouacs the next morning before the ants raid again. To date, twenty one different “bivouac-checking” bird species have been identified.

Tracking army ant bivouacs is more complicated than one might think. As the ants raise their young, they cycle through two distinct phases: one (approximately 20-day) phase during which they remain in a set location, conducting most of their raids at the beginning and end of the phase and relatively few during the middle two weeks; and a second (approximately 14-day) nomadic phase, during which they move their bivouac on a daily basis and conduct raids almost every day.

Aren’t you hungry? We haven’t eaten since tomorrow. (Ocellated Antbirds, credit PhilSlosberg)

From the perspective of a bivouac-checking bird seeking a reliable food source, these varying phases are significant. When the ant colony is stationary, it may be relatively easy to find, but its raids will be sporadic; when the colony is nomadic, it may be more difficult to find, but its raids will be quite regular. Clearly, a bird will do better if it can keep track of multiple stationary colonies that conduct raids only sporadically, if it can quickly find nomadic colonies based on their prior locations and previous movements, and if it can remember whether particular colonies are in phases in which they’re likely to conduct raids.

The researchers identified these conditions as providing a potential testing ground for MTT. While the birds obviously can’t be interviewed, their environment may elicit behavior that shows that they have an “episodic-like memory” (that is, they can recall the what-where-when aspects of past events) and that they can take action in anticipation of future motivational states independent of their current needs (that is, they can plan flexibly for the future).

After noting that the birds appear to form specific memories about locations (since they return in the morning after evening bivouac checks), the researchers hypothesize that the birds may remember which colonies are in which locations and what phase the colony is in, “and that they may be using episodic-like memory if they prefer to check those bivouacs from army ant colonies in the nomadic phase.” Moreover, they continue:

Time travel jokes never get old! (Spotted Antbird, credit Mike Danzenbaker)

We suspect that future planning could be involved in bivouac-checking bird behavior because birds check bivouacs when sated (conferring no immediate benefit), a behavior that does not make sense until the next morning on return to the bivouac when the bird finds the ants raiding again and encounters its next meal (a delayed benefit). Because bivouac checking occurs after foraging at a raid, there is no immediate benefit to conducting this behavior in terms of acquiring a meal in the next few minutes. Instead, the benefit occurs the next morning when the ants begin raiding again; bivouac-checking birds return and are the first to begin foraging at the raid. This could indicate a dissociation between their current state (sated) and a future need (will need to eat tomorrow), which suggests anticipation of future events. (Citations omitted.)

Logan and her colleagues call for additional field research and, if their hypotheses are supported, laboratory experiments that will enable experimenters to vary bivouac locations and colony phases under controlled circumstances, and to determine whether the birds use specific memories and flexible future planning or whether they engage in automatic behavior using vision, smell, circadian rhythm or other cues in checking on bivouacs.

At this point, the researchers’ hypotheses need additional experimental support, but it’s already clear that they’ve made some keen observations about specialized behavior in the wild and have opened the door to substantially expanded testing for mental time travel in animals. As more researchers come up with similarly elegant ways of investigating abilities previously thought to be unique to humans, I think we will see additional barriers fall.

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1As regular readers know, this is a recurrent AnimalWise theme. Time and again we humans have claimed that we are the only ones to have a particular skill, only to discover later on that, in fact, many animals may share the same or comparable abilities with us. Prior posts have discussed this phenomenon in areas including tool use (many different fish, crested rats, ants, dolphins, chimpanzees, crows), language (bees and prairie dogs), analogic reasoning (capuchins and baboons), grief and mourning in various animals, and self-recognition (dogs, magpies).

ResearchBlogging.org2Logan, C., O’Donnell, S., & Clayton, N. (2011). A case of mental time travel in ant-following birds? Behavioral Ecology DOI: 10.1093/beheco/arr104.

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The Wisdom of the Aged: Matriarch Elephants Lead with Experience

As many people know, African elephants (Loxodonta africana) live in complex matrilineal societies, with closely-knit family groups led by a matriarch who is typically the oldest and largest female in the family. In order to appreciate the importance of these matriarchs, it may help to first consider a traditional Japanese folktale:

Once there was an arrogant young village lord who, deciding that old people were useless, banished them to the mountains to die. Although the villagers were distressed, they obeyed rather than face severe punishment. One young farmer couldn’t bear to follow this cruel decree, though, and hid his aged mother away in a safe and secret room.

Several years later, an invader arrived, announcing that he’d spare the village only if three tasks could be performed. First, he must be presented with a box containing one thousand ropes of ash. Next, a silk thread must be drawn through a small hole that bent seven times along the length of a log. Finally, he must be given a drum that sounded without being beaten.

In each case, the village lord offered rewards, cajoled and threatened the townspeople, but nobody knew what to do; all were in despair. The tasks all seemed impossible. Each time, though, the farmer asked his mother and she knew the answer: soak ordinary rope in salt water before burning it; tie the silk thread to an ant at one end of the hole and place sugar at the other; put a bumblebee in a drum and it will buzz as it tries to escape. The village was spared.

Ultimately, the lord finds out that they have all been saved by the wise old mother, and from that time on elders in the village are revered.

Shifting scenes now from the mountains of long-ago Japan to the plains of today’s Africa, it turns out that older matriarch elephants are much like the heroic old Japanese mother – they are the ones with the answers, the ones that can save their fellow elephants from outside threats with the wisdom they have accumulated through experience.

Listen to your Grandmother! (image copyright ElephantVoices)

As we know from the decades of observation and research performed by Cynthia Moss and her colleagues in Kenya and Tanzania, matriarch elephants act as group leaders, holding together their families and providing behavioral guidance during times of crisis. Many observers believe that the oldest matriarchs – those with the most experience and greatest ecological knowledge – make the best decisions, but until recently it has proved to be difficult to quantify the relevant skills in a manner conducive to experimental testing.

In a March 2011 paper published online in the Proceedings of the Royal Society B, however, a team of scientists led by Karen McComb of the University of Sussex reported on a clever set of experiments that tested whether older Amboseli National Park matriarchs were better than their younger counterparts at assessing the perceived threat posed by various lion roar recordings.

While African elephants are able to fend off most natural predators, they have to watch out for lions, who occasionally prey upon younger calves. Also, even though lionesses perform the, ahem, lion’s share of the hunting for the pride, male lions actually pose a greater threat to elephants. Male lions, despite their generally well-deserved reputation for laziness, are, on average, half again as large as females and much stronger, giving them a better chance of overpowering a vulnerable young elephant.

Accordingly, the researchers assembled lion “playbacks” in four separate categories – single female roars, single male roars, three female group roars and three male group roars – which they then played to 39 elephant family groups over a period of slightly more than two years. Because of the extensive demographic information compiled by the Amboseli Elephant Research Project, they knew the age of the matriarch in each of the 39 families.

After playing the different roars, the researchers analyzed video of the elephants’ responses, focusing particularly on the behavior of the matriarchs. They documented specific defensive reactions, including prolonged listening to the roars, whether the family bunched around the matriarch after hearing the roars, the speed and intensity of any bunching behavior, and whether the matriarch changed her direction and moved toward the source of the playback.

Here are two brief videos, one showing an elephant family reacting to lion roars and the other narratively describing the reactions as reflected in still images:

After recording all of the responses, the research team performed statistical analyses and sorted their results by matriarch age. They found that, while matriarch age did not have an impact on how the elephants reacted to varying number of lions (all elephant families consistently ratcheted up the intensity of their response when the number of lions roaring went from one to three), it did have a strong impact on the elephants’ response to the more serious threat presented by male lion roars, with male roars leading to more prolonged listening and intensive defensive bunching in families led by older matriarchs.

As the researchers put it:

Our work provides the first direct experimental evidence that older matriarchs are in fact able to make better decisions when faced with ecological challenges — in this case, the presence of dangerous predators. It thus bridges an important gap between theoretical predictions about how knowledge might be expected to affect leadership and empirical studies, which to date have been largely confined to observational accounts.

Based on these findings, I’m quite confident that the older matriarchs will do quite well on their next set of tasks involving burning ropes, crooked logs and drums. Now, if only that was enough to keep humans from invading their villages….

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ResearchBlogging.org

The Japanese folktale can be found, among other places, in The Wise Old Woman/retold by Yoshiko Uchida; illustrated by Martin Springett. ISBN: 0689505825.

McComb, K., Shannon, G., Durant, S., Sayialel, K., Slotow, R., Poole, J., & Moss, C. (2011). Leadership in elephants: the adaptive value of age Proceedings of the Royal Society B: Biological Sciences, 278 (1722), 3270-3276 DOI: 10.1098/rspb.2011.0168.

Rise of the Planet of the Ants

These days, we’ve been hearing quite a bit about a future in which humans find their dominion over the planet suddenly challenged by a group of super intelligent apes. This may make for an exciting Hollywood movie plot and some stunning visual effects, but I wonder whether we really need to look to humanoid science fiction in order to feel a shiver of doubt regarding our supremacy as a species.

Maybe all we need to do is to look at the world the way it is, a world that could well be called … The Planet of the Ants!

So, why is it that we should feel just a wee bit threatened by these small six-legged colonizers? Here are just a few reasons.

Quadrillions of Ants

Burning Man seems more crowded every year, doesn't it? (photo credit: Mehmet Karatay)

Like us, ants thrive just about anywhere, with the exception of Antarctica and a few isolated islands. Moreover, while there are approximately seven billion of us on the planet, conservative estimates put the number of ants at between one and ten quadrillion.1 That’s between 150,000 and 1,500,000 ants for each and every one of us. At the higher figure, this means that, if you were to put all the world’s ants onto a giant scale, they would weigh about as much as all of the humans on the planet put together.2 In fact, on average, it has been estimated that ants make up 15–20% of the terrestrial animal biomass on Earth (and more than 25% of the animal biomass in tropical regions).3

Our tendency as humans is to unquestioningly assume that we are far and away the most successful species that has ever been. If we take a step back, though, and simply consider the above numbers and the possibility that an animal’s success is most properly measured by the degree to which it has been able to thrive in various environments, perhaps we should already be feeling a pang of doubt about how incontestable our supremacy really is.

Ants Teach

While many animals are able to learn through imitation, ants are the only non-mammal known to engage in interactive teaching.4 In at least one species of ant, knowledgeable workers actively teach inexperienced nest mates where to find food through a process known as “tandem running,” in which the lead worker ant recruits an inexpert follower, and then makes sure that the follower stays on track, slowing down when it lags and speeding up when it gets too close.

Ants Learn

Ants are also able to engage in so-called latent learning, whereby they memorize information that they cannot use at once, but that may be useful later on – a behavior that’s been labeled as “planning.”5 Specifically, ants have been shown to be able to reconnoiter potential new living spaces, retaining information about relative desirability and tailoring their choices based on how urgently the need to move is.

Ants Can Learn to Navigate Mazes

Ants can be trained to remember multiple visual patterns presented in a fixed sequence, enabling them to navigate mazes.6 Ok, I’m not sure how exactly this leads to world domination, but it is definitely pretty cool.

Ants Practice Agriculture

Approximately 50 million years ago (and, accordingly, approximately 49+ million years before Homo Sapiens first arose as a species), ants began engaging in agriculture.7 Today, different species of leafcutter ants have adopted a purely agrarian lifestyle, feeding exclusively on gardens of fungus that they actively weed and cultivate, feed with fresh-cut leaves, and keep free from parasites and other pests.8 Here’s a video of some fungus farming ants:

Ants Engage in Animal Husbandry

Some ants raise aphids and feed on the sugary honeydew the aphids secrete when “milked” by the ants’ antennae. The ants are careful with their herds, keeping predators and parasites away, moving the aphids from one feeding location to another, and often bringing the aphids with them when they migrate.9 Here’s a video of ants tending to their aphids:

Ants Sometimes Enslave Other Ants

Certain types of ants are incorrigible slave-makers, raiding other colonies of ants and making captured slaves perform all routine tasks for their masters, including brood care, foraging, and even feeding slave-maker workers who are unable to feed themselves.10 Obviously, this isn’t a particularly attractive ant characteristic, but unfortunately it is one that may seem all too familiar to us humans.

Ants Use Tools

That’s right, tools. For example, some ants transport liquid and other non-solid food by dropping bits of leaves, sand or mud pellets or pieces of wood into a pool of food and, after the food has soaked in, using these objects to carry the meal back to their nests.11 Other ants use pebbles and soil pellets as weapons, dropping them on other ants or ground-dwelling bees, and then attacking and killing their competitors.12

Ants Build Cooperative Solutions

Hey, watch your foot! You're stepping on my head! (photo: Mlot, Tovey & Hu)

Ants, including army ants, are known to self-assemble into living bridges or ladders that allow them to cross gaps while on the move. When a single ant cannot make it across alone, other ants will successively grab on, steadily lengthening the bridge until it’s long enough to reach the destination. These structures, which can span significant distances and can even cross water, are then used by the rest of the colony and may stay in place for hours, until traffic dies down.13 Comparably, fire ants self-assemble into waterproof rafts to survive floods. These rafts can be made up from anywhere from a few hundred to many thousand ants and are incredibly durable, allowing ants to sail for months at a time as they migrate.

Ants Have “Collective Intelligence”

The concept of collective intelligence has been hot lately, with a number of books and articles describing how groups can make collectively make sophisticated decisions and solve complex problems, even where each individual in the group knows very little, collectively a g (think of the analogy of each individual acting as a neuron, and the group as a whole acting as a collective brain). Collective intelligence is a topic unto itself, one we may address in future posts, but for now suffice it to say that if ants truly can make wise decisions as a group, we humans may really have something to envy!

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ResearchBlogging.org1Holldobler, B & E. O. Wilson (2009). The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies. New York: W. W. Norton. p. 5. ISBN 0-393-06704-1.

2Ibid.

3Schultz, T. (2000). In search of ant ancestors Proceedings of the National Academy of Sciences, 97 (26), 14028-14029 DOI: 10.1073/pnas.011513798.

4Franks, N., & Richardson, T. (2006). Teaching in tandem-running ants Nature, 439 (7073), 153-153 DOI: 10.1038/439153a; Richardson, T., Sleeman, P., McNamara, J., Houston, A., & Franks, N. (2007). Teaching with Evaluation in Ants Current Biology, 17 (17), 1520-1526 DOI: 10.1016/j.cub.2007.08.032.

5Franks, N., Hooper, J., Dornhaus, A., Aukett, P., Hayward, A., & Berghoff, S. (2007). Reconnaissance and latent learning in ants Proceedings of the Royal Society B: Biological Sciences, 274 (1617), 1505-1509 DOI: 10.1098/rspb.2007.0138.

6Chameron, S., Schatz, B., Pastergue-Ruiz, I., Beugnon, G., & Collett, T. (1998). The learning of a sequence of visual patterns by the ant Cataglyphis cursor Proceedings of the Royal Society B: Biological Sciences, 265 (1412), 2309-2313 DOI: 10.1098/rspb.1998.0576; Reznikova, Z. 2008: Experimental paradigms for studying cognition and communication in ants (Hymenoptera: Formicidae). Myrmecological News 11: 201-214.

7Schultz, T., & Brady, S. (2008). From the Cover: Major evolutionary transitions in ant agriculture Proceedings of the National Academy of Sciences, 105 (14), 5435-5440 DOI: 10.1073/pnas.0711024105.

8Ibid.; Schultz, T. (1999). Ants, plants and antibiotics. Nature, 398 (6730), 747-748 DOI: 10.1038/19619.

9Nielsen, C., Agrawal, A., & Hajek, A. (2009). Ants defend aphids against lethal disease Biology Letters, 6 (2), 205-208 DOI: 10.1098/rsbl.2009.0743; Styrsky, J., & Eubanks, M. (2007). Ecological consequences of interactions between ants and honeydew-producing insects Proceedings of the Royal Society B: Biological Sciences, 274 (1607), 151-164 DOI: 10.1098/rspb.2006.3701.

10Pohl, S., & Foitzik, S. (2011). Slave-making ants prefer larger, better defended host colonies Animal Behaviour, 81 (1), 61-68 DOI: 10.1016/j.anbehav.2010.09.006; Brandt M, Foitzik S, Fischer-Blass B, & Heinze J (2005). The coevolutionary dynamics of obligate ant social parasite systems–between prudence and antagonism. Biological reviews of the Cambridge Philosophical Society, 80 (2), 251-267 PMID: 15921051; Hölldobler, B. & Wilson, E.O., 1990. The Ants, Harvard University Press.

11FELLERS, J., & FELLERS, G. (1976). Tool Use in a Social Insect and Its Implications for Competitive Interactions Science, 192 (4234), 70-72 DOI: 10.1126/science.192.4234.70.

12See, e.g., Pierce, J. (1986). A Review of Tool Use in Insects The Florida Entomologist, 69 (1) DOI: 10.2307/3494748.

13Mlot NJ, Tovey CA, & Hu DL (2011). Fire ants self-assemble into waterproof rafts to survive floods. Proceedings of the National Academy of Sciences of the United States of America, 108 (19), 7669-73 PMID: 21518911.

Multi-Modal Monkey Memory

Recognizing someone you know is actually not a simple cognitive task – it requires you interpret the information you’re currently receiving through your senses, and then link back to a previously-formed conceptual representation you have of the individual in question. It’s especially difficult if you are acting cross-modally, for example matching someone’s voice to a photograph or vice versa.

Oh yeah, I remember him. He's the one with the high squeaky voice, isn't he? (photo credit: Joe Kegley)

Recently, two separate studies have shown that rhesus macaque monkeys (Macaca mulatta) are quite up to this challenge, reflecting that they possess a considerable degree of social memory and engage in complex conceptual thinking about other individuals.

French Pictures

In the first study1, published earlier this year in Proceedings of the National Academy of Sciences, a French research team headed by Julian Sliwa of the University of Lyon confirmed that rhesus macaques are able to spontaneously match the faces of known macaques and humans to their voices.

In their experiments, the research team gave six macaques a large number of tests in which they played short voice samples of known individuals (coos and grunts for other macaques, short French sentences and phrases for humans) and then measured how long the macaques spontaneously looked at cropped photographs of two known faces, only one of which matched the voice they had heard. The researchers statistically analyzed whether the macaques spent more time looking at specific photos after hearing the matching voice than they did after hearing a different voice, and found that the macaques did indeed stare significantly longer at a photo – whether of another macaque or a human – if the matching voice had been played first.

In reviewing individual performance, the researchers observed that five of six of the macaques displayed this effect overall, and that a greater number were better at recognizing photos that matched human voices than ones matching the voices of fellow macaques (the researchers noted that they were surprised at this finding, but pointed out that perhaps the explanation was that there were more useful auditory cues in the human speech samples than there were in the monkey coo vocalizations). Finally, the researchers found that five of the six monkeys showed preferences for specific faces, spending an especially long time looking at matching” photos of certain individuals – often a “neighbor” monkey or the researcher who was their main caregiver.

The researchers concluded that rhesus macaques can recognize individuals, linking together abbreviated visual and auditory perceptual cues (small, two-dimensional photos and short sound samples) to spontaneously identify other macaques and socially-relevant humans, and even to reflect the preference biases they have towards specific individuals.

At the Movies

The second study2, published last week in PLOS ONE, extended the findings to show that rhesus macaques can also recognize photos of other macaques whom they had seen during video clips, an additional challenge because specific features can be harder to identify in dynamic movies than in still images.

In this study, researchers led by Ikuma Adachi of the Yerkes National Primate Research Center began by training five macaques to watch brief silent video clips of familiar individuals before identifying which of five randomly placed photos represented the individual in the video. At first the macaques were allowed to continue to look at the last frame of the video before having to choose the correct photo, but in a second phase of the experiment the screen went black after the video was played, and the monkeys had to choose the correct photo after a time lag.

In each case the macaques became proficient at the task, even performing well after seeing videos taken from a novel perspective that was substantially different than the view in the training videos. Thus, their performance suggested that they were able to recognize specific features of known individuals as they appeared in dynamically-changing scenes in a range of videos, and then extract that information to identify those individuals later on in still images.

Next, the researchers repeated the testing, but this time they tweaked the conditions by playing a brief vocalization right after showing the last frame of the some of the videos – either a vocalization of the macaque in the video (the “congruent condition”) or of a different macaque (the “incongruent condition”). Only two of the macaques participated in this testing, as apparently the other three weren’t comfortable with working in the sound isolation booth necessary for this phase.

The researchers found that the macaques, who had never been trained to use vocalizations to guide their test responses, continued to be good at choosing the “correct” photo, but that when they made errors, they were statistically more likely than chance to pick the image of the vocalizing monkey, rather than the one in the video.

In other words, hearing the vocalizations systematically biased the macaques’ choice behavior, indicating that the voices may have activated visual representations of the vocalizing monkeys that occasionally superseded the impact of what had been seen in the video. Again, the macaques were demonstrating how they processed the information they used to recognize information cross-modally.

So, clearly “see no evil” is linked to “hear no evil” – perhaps we’ll see how “speak no evil” fits into the picture in a later post.

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ResearchBlogging.org

1Sliwa J, Duhamel JR, Pascalis O, & Wirth S (2011). Spontaneous voice-face identity matching by rhesus monkeys for familiar conspecifics and humans. Proceedings of the National Academy of Sciences of the United States of America, 108 (4), 1735-40 PMID: 21220340.

2Adachi, I., & Hampton, R. (2011). Rhesus Monkeys See Who They Hear: Spontaneous Cross-Modal Memory for Familiar Conspecifics PLoS ONE, 6 (8) DOI: 10.1371/journal.pone.0023345.

The Honeybee Waggle Dance – Is it a Language?

The Dance

More than half a century ago, Karl von Frisch rocked the world of behavioral biology with his conclusion that the honeybees (Apis mellifera) can actually communicate the distance to and direction of valuable food sources through an elaborate “waggle dance.” In what later led to his receipt of the Nobel Prize in Physiology or Medicine, von Frisch determined that bees recruited by this dance used the information encoded in it to guide them directly to the remote location of the resource.

In the typical waggle dance, a foraging worker bee who has found by a rich food source returns to the hive, is greeted by other bees, and commences dancing on the vertical comb surface within the dark nest (in other species of bee, like Apis florea, the dance is performed on a horizontal surface in direct view of the sun and/or other landmarks). She dances in a figure-eight pattern, alternating “waggle runs,” during which she vigorously waggles her body from side to side in a pendulum motion at about 13 times per second as she moves forward in a straight line, with return phases in which she circles back to the approximate starting point of the previous waggle run, alternatingly between clockwise and counter-clockwise returns. Here’s a video of a bee doing the waggle dance:

As the video indicates, the honeybee’s dance encodes key information about the resource. For instance, as she performs waggle runs on the vertical comb surface, her average body angle with respect to gravity corresponds to the direction of the food source relative to the current position of the sun (the sun’s azimuth). Accordingly, if the food source lies in the exact direction of the sun, she will waggle straight upwards; if the food lies, say, 30 degrees to the right of the imaginary line to the sun, she will angle upwards 30 degrees to the right of vertical. Also, the duration of her waggling runs is directly linked to the flight distance from the hive to the food source, with (for many bee subspecies) every extra 75 milliseconds of waggling adding roughly another 100 meters to the distance. Further, the more attractive the destination, the longer and more vigorously she dances, and the more quickly she returns for the start of each waggle run. Depending on the richness of the food source, she may perform up to 100 waggle runs in a single dance.

Next week ... the Tango!

Cognitive Complexity

It seems, then, that honeybees have evolved an extraordinary complex form of symbolic communication about distant resources, one that is beyond the capabilities of virtually every other species except for humans. Not bad for an insect.

The cognitive tasks implicated by the waggle dance are not insignificant: the dancer must remember the location and characteristics of a specific site she has seen on her foraging trips, and translate this information into the appropriate dance characteristics. She must also remember and take into account the position of the sun, and update that position as the sun moves (the ability to compensate for the sun’s movement by memory has been documented by researchers observing dances over several hours of overcast weather, when there are no celestial cues to be seen). The observing bees must “read” the dance, translate their sensory input into a resource location, and then find the resource, navigating as necessary around hills, houses and other obstacles.

In fact, the feat is so stunning that von Frisch’s findings were initially met with significant skepticism and controversy.1 At this point, the controversy has essentially been settled, with scientists recognizing that there is compelling evidence that honeybees really do communicate and act on the information encoded in the waggle dance, even though uncertainty remains regarding exactly which signals (tactile, odor, vibrations, air flows, etc.) the observing bees use to translate the dance into actionable information regarding the resource location.2

Is the Waggle Dance a “Language”?

So, the waggle dance is an extremely complex communication system, but is it a language?

Eileen Crist, Associate Professor in Science and Technology in Society at Virginia Tech, makes a rather compelling case that the waggle dance embodies many of the attributes of a true language.3 After noting that the waggle dance is always performed in front of an audience and is clearly communicative in nature, she describes some of the principal features that support its being characterized as a language:

  1. Rule-Governed. If a communication system is to be considered linguistic in nature, it generally must be based on a set of rules that are structured and used with regularity. This is the case with the waggle dance: the dance is always performed in a designated place within the hive, it is never done unless an audience is present, and it always follows a standard template for conveying direction, distance, and desirability. While the general rule is that the waggle dance is to be used to inform other bees about sources of nectar, when the colony has a special requirement (e.g., locating water when the hive is overheating or finding a new home when part of the colony must relocate) then the rules dictate that the dance purpose switches to this pressing need. Also, the general rule is that foragers dance about rich, reliable and near resources, but in times of need the “dance threshold” for less desirable resources is lowered.
  2. Complexity. A key dimension of a true language is its complexity, as it is unlikely that a communication system based on just a few rules will qualify as a language. The bee dance rules are not only extremely intricate, but they are applied in a versatile and complex fashion to respond to differing environmental factors and hive requirements.
  3. Stability and Dynamism. A core feature of human language is that a relatively fixed and stable syntax enables the dynamic generation of an indefinite number of new sentences. Similarly, while the waggle dance always takes the same recognizable forms, it “accommodates different purposes, shifting circumstances, urgent needs, and unprecedented events; while structurally identical every time, it is also contextually flexible.”
  4. Symbolic. By itself, the symbolic nature of the waggle dance has led to its being called a language. The dance symbolically represents conditions existing in the real world, actually enabling human researchers to “read” the information encoded in the dance to find specific honeybee food sources and even to design experiments about honeybee foraging behavior.
  5. Performative. According to linguistic theory and as first articulated by John Austin, languages not only describe the world, they also include what he called “performative” utterances, which are used to carry out actions.4 Not only is the waggle dance symbolically descriptive, but it has performative force in the sense that it elicits action from the bees who watch it (as Crist notes, the performative nature of the waggle dance is implicit in the way in which scientists “routinely deploy a vocabulary of announcing, reporting, summoning, recruiting, soliciting, inviting, commanding, and guiding” in describing it).

James Gould, Professor of Ecology and Evolutionary Biology at Princeton University, summarized both the controversy over the issue and the nature of honeybee dance communication as follows:

Some of the resistance to the idea that honey bees possess a symbolic language seems to have arisen from a conviction that “lower” animals, and insects in particular, are too small and phylogenetically remote to be capable of “complex” behavior. There is perhaps a feeling of incongruity in that the honey bee language is symbolic and abstract, and, in terms of information capacity at least, second only to human language.5

Gould estimates that the waggle dance is capable of communicating at least 40 million unique messages (“sentences”), more than 10 times as many as any other animal except for man.6

Not surprisingly, not everyone agrees that the waggle dance constitutes a true language. For example, Stephen Anderson, Professor of Linguistics at Yale University, acknowledges that honeybee dance communication is elaborate and cognitively rich, but concludes that it is unlike human natural language in that, for example, it is genetically fixed rather than learned through environmental interactions, it lacks a syntax in which the order of the communicative elements (words or actions) impacts meaning, and there is a close correspondence between the structure of the dance signals and the nature information to be conveyed (e.g., orientation of the waggle run and the direction to the resource).7

Some bees are better at the dance than others...

To Bee or Not to Bee

In the end, there will probably always be debate and disagreement over whether the waggle dance is a true language. Clearly, the waggle dance and human language are vastly different communication systems, and how we label the waggle dance in human terms may be missing the point. From the honeybee standpoint, the dance serves its purposes and contains all of the communicative nuances that the bees need within their environment. Maybe, the real point is that we should sit back and appreciate the fact that the honeybee, a small insect with tiny brain, has been able to evolve a system of communications that is so sophisticated that it has challenged human linguists to wrestle with the question of what distinguishes a true language and whether human language is really so unique.

Anyhow, time to stop droning on and sign off!

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1See, e.g., Gould, J. (1975). Honey bee recruitment: the dance-language controversy Science, 189 (4204), 685-693 DOI: 10.1126/science.1154023.

2See, e.g., Landgraf, T., Rojas, R., Nguyen, H., Kriegel, F., & Stettin, K. (2011). Analysis of the Waggle Dance Motion of Honeybees for the Design of a Biomimetic Honeybee Robot PLoS ONE, 6 (8) DOI: 10.1371/journal.pone.0021354; Gil, M., & De Marco, R. (2010). Decoding information in the honeybee dance: revisiting the tactile hypothesis Animal Behaviour, 80 (5), 887-894 DOI: 10.1016/j.anbehav.2010.08.012.

3Crist, E. (2004). Can an Insect Speak?: The Case of the Honeybee Dance Language Social Studies of Science, 34 (1), 7-43 DOI: 10.1177/0306312704040611.

4Hymes, D. (1965). : How to Do Things with Words . John L. Austin. American Anthropologist, 67 (2), 587-588 DOI: 10.1525/aa.1965.67.2.02a00970.

5Gould, J. L. Ibid. at 692.

6Gould, J. L. Ibid. at note 37.

7Anderson, S. R. 2004. Doctor Dolittle’s delusion: Animals and the uniqueness of human language. New Haven, Conn.: Yale University Press. ISBN-13: 978-0300115253.

Pantomiming Primates

When considering language abilities in non-human animals, it pays to keep in mind that spoken words are not the only path to sophisticated communication. For example, while great apes like chimpanzees and orangutans may be limited in their ability to adapt their vocalizations to human speech, they are able to control their hand movements very well, and can engage in extremely expressive and effective gesturing behavior.

In a thought-provoking study first published online last year and now appearing in the August 23, 2011 issue of Biology Letters1, two Canadian researchers, Anne Russon of Glendon College and Kristin Andrews of York University, reported on their extensive review of data regarding instances in which orangutans in Borneo have used “pantomime” to communicate with their target audiences.

What part of "give me more food" don't you understand? (photo credit: Tom Low)

Russon and Andrews mined 20 years’ data that had been collected during systematic observational studies on the behavior of ex-captive orangutans as they underwent rehabilitation and were living free or semi-free lives in the forest. After reviewing original field notes and videos covering over 7,000 hours of observation, they identified 18 salient pantomime cases (14 addressed to humans and four to other orangutans) in which orangutans physically acted out messages in order to communicate specific goals.

In most of the cases, the orangutans used pantomime to provide additional or better information after an initial attempt at communication had failed – for example, by being more specific about an action, item or tool requested; by offering better tools for a requested task after a previous tool had been ignored; by pretending to be unable to perform a task after a request for help had been ignored; or by clarifying friendly intent after non-aggressive approaches had been refused.

A few specific examples will help to illustrate how the orangutans used pantomime to achieve specific communication goals:

  • An adolescent female named Siti, who had partially opened and eaten a coconut, handed it to a technician who in turn handed it back to her, gesturing to her that she should finish the job. She proceeded to briefly, weakly and ineffectively poke at the coconut (very much in contrast to her prior behavior), before handing it back to the technician. When he again refused to help her, she used a palm petiole (stalk) to chop at the coconut repeatedly, as one would with a machete. Russon and Andrews described their interpretation of the incident in the data supplement to their paper:

After [the technician’s] first refusal she faked inability to do the job herself; after the second refusal she elaborated her request by acting out what she wanted done, specifying what tool and target to use and how to use the tool.  She acted out the actions she wanted of her partner, which included a skill that was not in her own repertoire (machete use).  Given the complex conjunction of conditions and the specificity of her request, Siti’s pantomime must have been invented on the spot even if she was familiar with all constituent elements.

Fortunately, you can see this incident for yourself, as there’s a video of Siti and the coconut – enjoy!

  • After a three year old female named Kikan had hurt her foot on a sharp stone, a research assistant removed the stone and dripped latex from the stem of a fig leaf on the wound to help make it heal faster. After that, Kikan (who had previously not been particularly friendly with the assistant, hitting or trying to bite her when she passed by) approached the assistant in a friendly manner on a number of occasions, holding up her wounded foot for the assistant to see. On one specific occasion, Kikan picked up a leaf, pulled the assistant’s hand until she paid attention, and then acted out the leaf treatment the assistant had given to the foot. (This is not only interesting for its communication content, but it could be an indication of episodic-like memory (mental time travel), a topic that Felicity Muth recently discussed in some detail in two Scientific American blog posts, here and here).
  • An adult female named Unyuk played with forest assistant who pretended to give her a haircut with a Swiss Army Knife. While they played she noticed a backpack, an item regularly stolen by orangutans in hopes of finding food. Unyuk made no immediate move for the pack – instead she continued to act out her role in the haircutting game, grabbing the hair on top of her head and inviting the assistant to continue playing as she gradually moved sidewise and closer to the pack. Once she had a free path, she lunged and made a grab for the unattended pack. (This was one of seven pantomimes that the researchers labeled as deceptive, where the actor feigned an inability, an interest or an intent in order to obtain help, distract, or express friendly intent and facilitate reconciliation.)

Russon and Andrews believe that some of the pantomime cases contain attributes of natural language:

including compositionality (large meaningful units are composed of smaller meaningful units…), systematicity (the actions and entities pantomimed are meaningfully rearranged following predictable patterns…) and productivity (…unique creations of the moment). Thus, orangutans can communicate content with propositional structure and have the kind of cognitive capacities with constituent structure typically associated with linguistic capacities.

Although spontaneous pantomiming appears to be fairly rare among orangutans (again, a total of 18 examples were unearthed from 20 years’ of data), the underlying data came from studies that were not focused on communication, and the researchers believe that other studies may have missed similar pantomiming to the extent that they focused on the functional aspects of gestures rather than the significance of pantomime as a medium for communication.

In any event, the study offers an eye-opening lesson in how sophisticated – to the point of being linguistic – non-verbal communication can be. If nothing else, we should not be too overconfident if we ever have a chance to play charades against a team of orangutans.

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1Russon, A., & Andrews, K. (2010). Orangutan pantomime: elaborating the message Biology Letters, 7 (4), 627-630 DOI: 10.1098/rsbl.2010.0564.

Asian Elephant Social Networkers

In a terrific new study in this month’s BMC Ecology1, a team of researchers led by Shermin de Silva of the University of Pennsylvania Biology Department has published the results of extensive, multi-year research regarding the social dynamics of a population of Asian elephants (Elephas maximus) at Uda Walawe National Park in Sri Lanka. The researchers studied 286 adult female elephants from September 2006 to December 2008, observing the social relationships they formed on a one-to-one basis, in small groups, and at the overall population level.

While group social behavior in African savannah elephants (Loxodonta africana) has been studied extensively, this new research is the first detailed, quantitative study of a wild Asian elephant population over such a lengthy time period … and what the researchers found was quite surprising.

You spend all your time social networking! First do your homework, then you can go on Facebook (photo credit: HelpElephants.com)

Prior less comprehensive studies had suggested that Asian elephants form less complex social networks than do African savannah elephants, with Asian elephants forming smaller and looser social groups based primarily on mother/daughter bonds, and rarely if ever involving relationships between unrelated females. In this in-depth longitudinal study, though, a different, more nuanced, portrait of Asian elephant society emerged.

Although, on any given day, the researchers would see only small groups of elephants that didn’t appear to interact extensively, over time, individual elephants formed larger social units that could be remarkably stable across years, even while associations among such units varied quite a bit across seasons.

One-to-One Relationships (Dyads)

The researchers started out by measuring how much time pairs of adult females spent together and found that, at a high level, the frequency of their associations was highly correlated across all five seasons in the National Park (Sri Lanka has a highly seasonal environment, with two separate monsoon seasons, two dry seasons, and a transitional season) – that is, pairs who associated in one season tended to associate in all seasons, and those who did not associate in a given season weren’t likely to associate at all.

Yeah, let's just hang and make nice for now, then we'll hit the rice paddies when nobody's looking! (photo credit: EleAid.com)

In studying one-to-one relationships, the researchers turned their attention to 51 “core” elephants who they thought would provide particularly good data, since these elephants were observed frequently and during all seasons of the year. These elephants formed a total of 478 pair relationships, which the researchers divided out statistically as follows:

  • A total of six (1.3%) of the pairings were “strong” and stable relationships, as measured by the relative percentage of time these pairs spent together during all seasons. Nine of the elephants (17.6%) participated in relationships in this category.
  • A total of 433 (90.6%) of the pairings were “temporary,” with the association peaking during a single season (most of the peaks were in either the transitional or dry seasons). All 51 of the elephants had at least one relationship that fell into this category.
  • A total of 39 (8.2%) of the pairings were “cyclical,” with the associations peaking in frequency during the two dry seasons (interesting, the researchers did not find relationships where the peaks were during the two wet seasons). Thirty two (62.7%) of the elephants had relationships that were cyclical.

Next, the researchers analyzed whether the identities of an elephants’ preferred companions changed over time. Overall, they found that the elephants spent slightly more than 20% of their time with their long-term companions (the top five companions over five seasons) and slightly more than 30% of their short-term companions (the top five for the current season). On an individual level, there was quite a bit of variation: eight (15.7%) of the elephants maintained 4 to 5 of their top five companions for all five seasons, while 16 (31.4%) completely changed their top-five companions during the study.

The researchers cite the example of two elephants, Kamala and Kanthi, who spent nearly all their time together – they were part of the “K” unit (Kamala, Kanthi, Karin, Kavitha and Kalyani, but no Kardashians) that was particularly close – and contrasted this kloseness to an individual named “471” that had few stable companions. (I wonder if this was due to distress over only receiving a number for a name.)

Additionally, the researchers noticed that the elephants who had the most relationships tended to form weaker bonds with each individual partner, whereas those with relatively few pairings tended to spend a relatively large amount of time with each of their companions.

Hmm, these elephants are beginning to sound quite a bit like people…

Small Group Associations (Ego Networks)

At the next level up, the researchers studied so-called “ego networks,” social networks consisting of an elephant and all of the other individual elephants with whom she associated at least once. The researchers focused on 88 of the adult females who they observed in every season, and calculated five measurements for each: (1) the number of her direct companions, (2) the number of ties between the direct companions, (3) the total number of potential ties between each of these direct companions, (4) the ratio of actual to potential ties, and (5) the number of individuals within two degrees of separation of the subject (number of friends plus number of “friends of friends”).

(Note that, assuming at least one of the researchers is within five degrees of separation of Kevin Bacon, this would mean that the entire ego network would be within seven degrees of separation of Kevin Bacon.)

Without getting into the full statistical analysis, the researchers’ principal conclusion was that:

[W]hile a subject’s direct companions do change over time, she has a few that are almost always present; even those that are not present continuously may have been companions in previous seasons. Thus, individuals maintain long-term relationships with others even though they may be apart for one or several seasons and [the amount of time spent together is small].

In other words, the elephants remember their friends and reestablish their relationships even after having been apart for long periods.

Population Level

Finally, the researchers looked at the social structure of the entire population. They found that the elephants in the overall popular had an extensive and well-connected social network, and that the distinct social units within the population were two to three times larger than had previously been seen in the field. Moreover, they observed that many of the social units maintained their integrity across seasons, even as individuals switched units and the connections between the units changed.

For those of you who like to look at dot patterns, below is a colorful series of diagrams depicting the connections between elephants, measured at different societal levels and during different seasons (T1 is the transitional season, D1 and D2 are the dry seasons, and W1 and W2 are, you guessed it, the wet seasons):

Figure 5 from Research Paper

Recap

While the strength of the associations among these Asian elephants (as measured by percentage of time that individuals spent together) is generally a good bit lower than that of the associations among African savannah elephants, most of these elephants had a few strong ties as well as consistent ties that they maintained over several seasons. Further, the Asian elephants were hardly asocial – while their mix of companions did fluctuate over time, they often returned to a subset of preferred companions.

Moreover, through their years of observation and statistical analysis of the elephants at the population level, the researchers found that the elephants’ social units were much larger than had been observed in prior studies, and that these social units were more stable across the years than were the companions of individual elephants.

The researchers speculated that one reason for the surprising findings is that the elephants stay in touch in ways that are hard for humans to detect, allowing the elephants to maintain bonds and relationships that we fail to observe. For example, elephants can communicate acoustically over great distances, and often use scent to follow one another’s paths at night (and, for that matter, even when the other elephants would be in plain sight, at least from the human perspective).

Finally, the researchers are planning to perform a detailed genetic study of the population in order to analyze the degree to which relatedness impacts the social organization of Asian elephant society. We’ll be waiting!

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1de Silva, S., Ranjeewa, A., & Kryazhimskiy, S. (2011). The dynamics of social networks among female Asian elephants BMC Ecology, 11 (1) DOI: 10.1186/1472-6785-11-17.

Sheep: Barnyard Brainiacs

It turns out that sheep are far more intelligent than their reputation for barnyard slowness would lead one to believe. In recent research published in PLoS ONE1, Professor Jenny Morton of the Department of Pharmacology at the University of Cambridge and her colleague Laura Avanzo reported that domestic sheep can perform extremely well on tests of designed to measure cognitive abilities, possibly as well as any animal other than primates.

Professor Morton, who had been studying Huntington’s disease, wanted to find out whether transgenic sheep with a specific genetic defect might be useful in preclinical research regarding potential treatments for this neurodegenerative disease. Because Huntington’s is characterized by cognitive deterioration, Morton was particularly interested in seeing how well sheep would perform cognitively, since suitable research subjects for neurologic disorders like Huntington’s inevitably must undergo systematic cognitive testing relevant to the disease.

Accordingly, Morton and Avanzo devised a series of tests that they gave to seven female Welsh Mountain sheep, six of whom completed the whole study. No word on why all of the ungulate volunteers were female, although my guess is that the males were off rollicking around with male bottlenose dolphins who were avoiding sponge fishing duty.

Welsh Mountain ewe: wool-giver and five-time Jeopardy champion (photo credit: Vertigogen)

The Tests

The tests were designed to measure the ability of the sheep to perform in three areas (discrimination learning, reversal learning and “attentional set-shifting”), which are relevant to what the researchers refer to as executive function – that is, the “ability to learn associations between stimuli, actions and outcomes, and to then adapt ongoing behavior to changes in the environment.” While the sheep took a large number of very specific tests, the tests fell into the following general categories:

  1. Simple discrimination tests. Sheep must choose between two feed buckets that are identical except one is blue the other is yellow. One color contains a food reward; the other is empty. Later “retention tests” repeat the original tests after time has passed to see how well the sheep remember.
  2. Simple discrimination reversal tests. Sheep must relearn the correct answer after sneaky researchers reverse the color of the bucket containing the food reward. (Note: we encountered this type of testing in the earlier AnimalWise post about the clever Anole lizards). Again, later “retention tests are given.
  3. Compound discrimination tests. The rewarded color is the same as in 1 above, but the relevantly-colored objects are now “perforated sports cones” rather than buckets. Additional buckets of irrelevant colors (one black, one green) are placed next to the sports cones, with the food reward in whichever bucket happens to be next to the correctly-colored sports cone.
  4. Intradimensional shift tests. Now, the sheep are presented with new shapes (rhomboids and cones) and new colors (purple and green). The sheep must still make a correct choice based on color, but need to learn the new color to apply.
  5. Intradimensional shift reversal tests. Same as 4, but sheep must relearn correct answer after the researchers change the rewarded color.
  6. Extradimensional shift tests. Again, the sheep are presented purple or green cones or rhomboids, but this time they must figure out now that the reward is based on choosing the correct shape, rather than a particular color.
  7. Extradimensional shift reversal test. Same as 6, but sheep must relearn after researchers swap which shape is rewarded.

Of the above tests, 1 & 3 measure “discrimination learning”; 2, 5 & 7 measure “reversal learning”; and 4 & 6 measure “attentional set-shifting.”

The Results

In a nutshell, the sheep did amazingly well.

They very quickly learned to pass the initial simple discrimination test (within seven sets of eight discriminations). When presented with the first reversal test, their performance initially dropped off, but they learned the new correct answer within three days of testing (11 sets of discriminations). For the compound discrimination testing, their performance again dropped slightly at the outset, but within two days they had this new puzzle figured out as well. Moreover, the retention tests showed that the sheep were able to remember the correct answer after time had passed (six weeks in the case of the simple discrimination test; two weeks for the simple reversal test).

At first, the sheep performed no better than chance on the more difficult intradimensional shift test, but they soon were performing at over 90% correct. They also experienced a large drop off in performance on the extradimensional shift test, but improved gradually until they reached 80% correct on the fourth day of testing. The sheep learned also were able to learn the reversals (within eight sets of discriminations for the intradimensional reversal and within 10 sets for the extradimensional reversal).

Morton and Avanzo summarized the results as follows:

We show that not only can normal can sheep perform discrimination reversal learning tasks, but they can also perform attentional set shifting tasks that test executive function. To our knowledge, this is the first time that these executive functions have been demonstrated in any large animal, apart from primates.

They were surprised by this success, conceding that they hadn’t been expecting the sheep to do well on the more difficult tests and indicating that they were “driven more by curiosity than expectation” in even giving the tests to them.

So, given these results, sheep seem to have gotten a bum rap for intelligence. There are relatively few studies on ovine intelligence, although research has shown that they can learn and remember how to navigate complex maze2 and that they are very good at remembering faces3.  And then there’s my favorite, that they’ve learned to roll their way across hoof-proof metal cattle grids in order to raid villagers’ valley gardens4!

One reason for the mistaken impression about sheep cognition may be that we have a bit of a blind spot when it comes to intelligence. We expect it in ourselves and a few other select animals, but even scientists can be quite surprised when it pops up elsewhere. Perhaps the main lesson here is that we should do our best to remain open to finding intelligence in unexpected places – if nothing else, this sort of a mental stretch will be a good test of our own cognitive abilities.

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1Morton, A., & Avanzo, L. (2011). Executive Decision-Making in the Domestic Sheep PLoS ONE, 6 (1) DOI: 10.1371/journal.pone.0015752.

2LEE, C., COLEGATE, S., & FISHER, A. (2006). Development of a maze test and its application to assess spatial learning and memory in Merino sheep Applied Animal Behaviour Science, 96 (1-2), 43-51 DOI: 10.1016/j.applanim.2005.06.001.

3Kendrick, K., da Costa, A., Leigh, A., Hinton, M., & Peirce, J. (2007). Sheep don’t forget a face Nature, 447 (7142), 346-346 DOI: 10.1038/nature05882.

4See, e.g., BBC News, “Crafty sheep conquer cattle grids,” July 30, 2004.

Portia, Queen of Spiders

Do you think that spiders are mindless machines, driven by pure instinct to make their webs and then attack intruders? Well, it’s time you met Portia:

The formidable Portia! (photo credit: Akio Tanikawa)

In an emerald rainforest of northeastern Australia, a sunbeam pierces the canopy, touches broad green leaves on the way down, and beams onto a lichen-spotted rock surface. In the beam’s circle, the slow, careful motions of a brownish jumping spider are illuminated. The jumping spider belongs to the genus Portia and it is stalking its prey, a different species of spider sitting in its own web. Portia steps cautiously from the rock surface out onto the web and stops. Delicately, Portia begins to pluck the web with its palps and legs, making signals that mimic the struggles of a trapped insect. When the prey spider ignores Portia’s plucking, Portia varies the characteristics of the signals, generating a kaleidoscopic of what appears to be a random selection of signals. Eventually, in response to one of these signals, the prey spider swivels toward Portia. Immediately, Portia backtracks to that particular signal and repeats it again and again. There being no further response from the prey, Portia eventually reverts to broadcasting a kaleidoscope of signals. When the prey spider still moves no farther, Portia adopts another ploy.

Now Portia slowly and carefully stalks across the web toward the resident spider, intermit­tently making a variety of signals. From time to time, a soft breeze blows, ruffling the web. The ruffling creates background noise in the web, and Portia exploits these moments, during which the resident spider’s ability to detect an intruder is impaired, by stalking faster and farther during these periods than when the air is still. Nearing the resident spider, Portia makes a signal that elicits from the resident spider a sudden, rapid approach. However, the spider advances very aggressively, and Portia scrambles to the edge of the web, then turns around to look over the scene. Soon Portia moves away from the web and undertakes a lengthy detour, first going away from the prey and around a large projection on the rock surface, losing sight of the prey spider along the way.

About an hour later, Portia appears again, but now is positioned above the web on a small overhanging portion of the rock. After anchoring itself to the rock with a silk dragline, Portia next slowly lowers itself down through the air, not touching the web at all. Arriving level with the resident spider, Portia suddenly swings in, grabs hold of the unsuspecting spider, and sinks its poison-injecting fangs into the hapless victim.

I’m going to leave the light on tonight, too.

This rather dramatic account is from a chapter in The Cognitive Animal written by Stim Wilcox (Department of Biology, SUNY Binghamton) and Robert Jackson (Department of Zoology, University of Canterbury, New Zealand)1.

For those of you who like visuals, here’s a brief video of Portia:

Clearly, you don’t want to mess with Portia.

In their essay, Wilcox and Jackson note how tricky it is to discuss cognition in animals, with almost as many definitions of the term as people using them. Rather than trying to choose a single definition, they instead apply a framework designed to raise questions about six separate cognitive properties: reception (taking in information), attention (focusing on particular tasks), representation (maintaining a mental image or cognitive map), memory (retaining information), problem solving (deriving pathways to the achievement of goals), and communication language (influencing other individuals by manipulating symbols).

They then run through these properties point by point, in the process illustrating the cognitive abilities of Portia.

Reception: In this area, Wilcox and Jackson emphasize Portia’s amazing eyesight, which apparently is more acute in distinguishing spatial features than that of any known animal of comparable size and even rivals that of primates: “Portia can precisely locate and identify spiders from a distance of 30–40 body lengths away, monitor the spider’s orientation and behavior during the course of a predatory sequence, and in general quickly gain critical information for predatory decisions during complex interactions with a dangerous prey.” For an in-depth article on Portia eyesight, you can check out this piece2 by Jackson and Duane Harland (I love the title: “‘Eight-legged cats’ and how they see”).

Attention: Wilcox and Jackson highlight the extraordinary, prolonged attention paid by Portia as she hunts, especially as she singles out and zeros in on a prey spider in an extended bout of stalking that involves multiple tactics and focused flexibility over time. They note how she must be particularly attentive, given the extreme sensitivity of her prey’s own web to movement and weight, and describe how she manipulates the signals she sends across the target’s web (aggressive mimicry) and opportunistically takes advantage of wind-caused background noise and vibration to move more quickly across the web than she does when the air is still (smokescreen tactics).

Representation, Memory, Problem Solving: For these areas, Wilcox and Jackson point to her planned detours, which demonstrate problem-solving and suggest mental maps and prolonged memory. They observe that, by planning ahead and formulating a solution before executing her maneuver, Portia comes particularly close to what we might typically call “thinking.”

Communication: Finally, while acknowledging that Portia clearly does not have any sort of verbal language or use symbols with arbitrarily assigned meanings, Wilcox and Jackson describe the way in which Portia strings together series of signals as she engages in aggressive mimicry, noting how this involves a complex, flexible and dynamic sequence of interactions between her and her target. As they put it, “Studying Portia’s signal-making strategy from this perspective may bring us closer than we initially expected to something like the cognitive implications of verbal language.”

I don’t have much to add here.  Hail Portia!

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1Wilcox, S. and Jackson, R. (2002). Jumping Spider Tricksters: Deceit, Predation, and Cognition. In M. Bekoff, C. Allen & G. Burghardt (Eds.). The cognitive animal: Empirical and theoretical perspectives on animal cognition. pp. 27–33. Cambridge, MA: MIT Press.

2Harland, D. and Jackson, R. (2000). ‘Eight-legged cats’ and how they see – a review of recent research on jumping spiders (Araneae: Salticidae). Cimbebasia 16: 231–240.

Perchance to Dream…

Do you ever wake up and feel like you’ve spent the whole night replaying a tape of the stresses of the day before? Well, at least you didn’t spend you didn’t spend that day running through mazes. Oh, you did? In that case, you might want to grab a chunk of cheese and sit down for some comfort eating with a friendly rat who can commiserate with you.

Matthew Wilson, an MIT professor of neuroscience, has been studying rats as they work and sleep for years, and has found out that they, too, replay their daily activities as they sleep.

Rat dreaming of running in circles... (MIT image)

In groundbreaking research published in 2001 in the journal Neuron1, Wilson and his colleague Kenway Louie were given an unprecedented glimpse into the dreams of rats by studying rats’ brain activity while they ran through mazes and then later on while they slept. (To clarify, the rats – not the researchers – were the ones who ran through the mazes. Sorry to disappoint you.)

To investigate what happens in the brain during rapid eye movement (REM) sleep, the type of sleep associated with dreaming, the researchers recorded the activity of neurons in the hippocampus (the area of the brain known to be critical to the formation and encoding memories) of four rats, both while the rats ran around circular mazes and then afterwards during REM sleep.

What they found out was striking.

As the rats ran through the mazes, the neurons fired in distinctive patterns that were dependent on where the rats were within the mazes. Then, when the researchers took comparable measurements of the rats’ brain activity later on during the rats’ REM sleep after a hard day of maze running, they found that the rats played back exactly the same neuron activity patterns as had occurred when they originally performed their tasks. More specifically, in 20 of the 45 REM sleep sessions that the researchers measured, they could detect prolonged periods (tens of seconds to several minutes in length) during which the same spatially-correlated hippocampal neurons fired in the same order, with the REM patterns essentially repeating the daytime patterns at approximately the same speed.

During REM sleep, we could literally see these rat brains relive minutes of their previous experience. It was like they were watching a movie of what they had just done.

In his terrific blog The Frontal Cortex2, Jonah Lehrer noted that Wilson was astonished by these results, quoting him as saying, “During REM sleep, we could literally see these rat brains relive minutes of their previous experience. It was like they were watching a movie of what they had just done.”

Wow!

More recently, Wilson and Daoyun Ji, a postdoctoral associate, extended these findings in research published in Nature NeuroScience3. In this newer study, the researchers focused on brain activity during slow-wave sleep (SWS), often referred to as deep sleep, a stage of sleep not characterized by dreaming but thought to be important to long-term memory formation. The researchers wanted to learn more about how the brain consolidates long-term memories during SWS, and whether it replays visual images from daytime experiences as part of the process. To test these matters, the researchers focused on the interaction between two separate areas of the brain: the hippocampus and the visual cortex, which is responsible for processing visual information.

As before, the researchers measured brain activity in four (presumably different!) rats as the rats ran in alternating directions through figure-eight shaped mazes, and then repeated the same measurements while the rats slept both before and after their maze-running sessions. This time, though, the researchers measured activity in both the visual cortex and the hippocampus.

Once again, the findings are notable.

As the rats ran through the mazes, neurons in both brain areas, the visual cortex and the hippocampus, acted similarly, firing in distinctive patterns that were dependent on where the rats were within the mazes. During subsequent SWS periods, the rats replayed these same firing patterns and sequences in both brain areas, much as they had done in the earlier experiment on hippocampus activity during REM sleep. Moreover, at all times, during maze-running activity and later on as the rats replayed their memories during periods of SWS, the brain activity in the visual cortex and the hippocampus were highly correlated.

By linking the visual cortex to this coordinated memory replay process, the researchers were thus able to show that not only were the rats replaying their daytime memories during sleep, but that they were reliving the same sensory experiences, the exact visual images that they had seen during their maze running!

Do these studies provide insight into the neurobiology of sleep, dreams and memory in humans and other animals? All mammals have similar brain structures that seem to operate similarly, and the research was designed to help us gain a better understanding of our own memory formation behavior, but it never hurts to ask these sorts of questions.

Assuming that these findings do have relevance for other species, then it may well be that when your Golden Retriever paddles his feet, rolls his eyes and twitches during sleep, he is indeed reliving that epic battle he recently had with an evil, slobber-covered tennis ball.

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1Louie, K., & Wilson, M. (2001). Temporally Structured Replay of Awake Hippocampal Ensemble Activity during Rapid Eye Movement Sleep Neuron, 29 (1), 145-156 DOI: 10.1016/S0896-6273(01)00186-6.

2The Frontal Cortex, “The Neuroscience of Dreaming,” December 19, 2006.

3Ji D, & Wilson MA (2007). Coordinated memory replay in the visual cortex and hippocampus during sleep. Nature neuroscience, 10 (1), 100-7 PMID: 17173043.

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