Canine Comprehension of Complex Communications

No question about it, canines are smart and adaptable. In recent posts, we’ve featured a dingo who cleverly figured out how to use a table as a tool enabling him to reach tempting food, described research suggesting that dogs may be so in tune with our feelings that they can catch yawning bouts from us, highlighted evidence that humans and dogs may be undergoing cognitive convergent evolution with each other based on our close social relationships over the millennia, and even noted a study pointing to canine self-awareness based on their recognition of their own, er, yellow snow.

Also, dog owners frequently describe how smart their cold-nosed friends are, how they know the words for large numbers of toys and other objects, and how they understand and sometimes obey numerous commands. (Good dog!) However, while there have been many studies investigating the linguistic abilities of primates, cetaceans, parrots and certain other species, there has been surprising little formal research into the verbal comprehension of dogs. Dogs have been tested for their understanding of specific words and commands, but there has been an absence of research into whether they can understand and distinguish the constituent parts of complex sentences that refer both to objects (e.g., “ball,” “stick” or “newspaper”) and to actions (e.g., “fetch,” “roll over,” or “point”).

Until recently, that is.

Chasing Down Linguistic Meaning

First, in 2011, John Pilley and Alliston Reid published a paper in Behavioural Processes detailing a variety of word comprehension tests that they had given to Chaser, a rock star border collie famous for knowing the names of over 1,000 objects.

In one of these experiments, Pilley and Reid tested whether Chaser could independently understand the meanings of verbs and nouns. In this test, Chaser was asked to respond appropriately when three different commands (take, paw, and nose) were randomly associated with three different stuffed cloth toys (Lips, a toy resembling human lips; ABC, a cloth cube with those letters written on its side; and Lamb, a stuffed lamb) in 14 independent trials using a double-blind procedure. Chaser was familiar with the commands, but none of the three toys had ever been paired with any of the commands prior to the experiment.

The three toys were lined up on a soft pad in front of a one-meter high cloth barrier. During the trials, neither Chaser nor the experimenter could see each other, as the experimenter knelt on one side of the barrier, with Chaser hanging out with the toys on the other side. The experimenter, who had been given a toy and command combination generated with a random number table, gave Chaser his instructions, while a confederate sat to the side where she could see Chaser perform and signal to the experimenter with a hand wave when the trial was over. Here’s a picture of the setup, taken before the experimenter retreated to the other side of the barrier to commence the trial (note that the confederate’s legs are visible to the right of the picture):

The tests were videotaped with sound recording, with three independent raters (not the experimenter or the confederate) scoring whether Chaser chose the correct toy and performed the correct command. Each rater first watched the videotape with the sound turned off (so he/she wouldn’t know which instructions had been given to Chaser), and recorded which command was actually executed towards which toy. After rating all 14 trials, the rater then watched each trial again with the sound turned on in order to assess whether Chaser’s behavior accurately matched the instructions given by the experimenter.

How did Chaser do? Perfectly.

There was absolutely no disagreement among the raters – each judged Chaser to be 100% accurate across the 14 trials, performing the correct command to the correct toy as instructed. As Pilley and Reid put it:

These results clearly support the conclusion that Chaser understood reference – that the verbal noun of an object referred to a particular object with distinct physical features independent of actions directed toward that object.

Comprehending Sentences

Then, earlier this month, Daniel Ramos and Cesar Ades of the University of São Paulo published a study in PLoS One that extended the Chaser research.

In their study, Ramos and Ades tested Sofia, a female mongrel dog, on two-item requests over a two year period, starting when she was a two-month old puppy. The testing consisted of eight progressive phases, during which Sofia first learned some basic vocabulary and then gradually faced increasingly complex tests of her comprehension abilities. The specific phases were as follows:

  1. Learn the names for four objects (ball, key, bottle and stick) and two requests (point or fetch).
  2. When presented with two objects, approach the correct object on request, or perform the correct action upon request.
  3. Perform object and action requests in sequence – that is, first approach the proper object after being given an initial “object request” and then, after being given an “action request,” perform the correct action on the object.
  4. Perform single multi-part requests – that is, after being given a compound request (e.g., ball fetch, ball point, key fetch, key point, bottle fetch and stick point), approach the correct object and perform the correct action.
  5. To eliminate the possibility of inadvertent cues from the experimenter, perform the same tests as in phase 4 but with the following control variations: (1) experimenter wearing sun-glasses, (2) experimenter with mouth covered by a cloth band, (3) research assistant absent from the room, (4) unfamiliar person as experimenter, (5) testing in an unfamiliar room, (6) test objects scattered, distant from one another, and (7) new objects of the same category (new balls, keys, etc.) offered.
  6. Perform reversed multi-part requests – that is, in response to compound requests in which the word order has been switched from object-action to action-object (e.g., fetch ball, point ball, fetch key, point key, fetch bottle and point stick), approach the correct object and perform the correct action just as in phase 4.
  7. Perform multi-part requests with a new, previously-untested object, a teddy bear.
  8. Perform multi-part requests with new combination object-action pairs (stick fetch and bottle point) that had not been used at all during prior training or tests.

And how did Sofia do? Well, she wasn’t perfect like Chaser, but she was pretty impressive. Her success rate was significantly above chance in all phases except for the final one, in which she had only 3 out of 10 correct responses for both the stick fetch and the bottle point requests. Notwithstanding this one area of underperformance, Ramos and Ades concluded:

Our results suggest that dogs share with “linguistic” animals the capacity to encode in memory at least two heterogeneous items of information to be used in subsequent directed performance, a capacity which, although far from being “an infinite use of finite means” as human grammars are, may have comparative relevance as a forerunner to syntactical functioning.

Now, I know what you are saying. Yes, your dog can do that too. I’m aware that she consistently beats you and your friends at poker, and I’ve seen the video where she plays charades while riding around your house on a Roomba.

You see, that’s actually the issue. Dogs are incredibly good at picking up human signals, which is why carefully-designed experiments are important in ruling out the “Clever Hans” effect (named after a horse who, more than a century ago, amazed crowds with his apparent mathematic abilities, but who was ultimately found to be picking up on involuntary body language cues from his trainer).

By eliminating visual contact between Chaser, Sofia and the experimenters and by adding controls such as having unfamiliar persons issue requests and moving around the objects, the researchers ensured that the dogs had to rely exclusively on words rather than on inadvertent human signals or other contextual clues. By changing the size, shape and color of the requested objects and introducing a new object (the teddy bear), the researchers were able to test whether Sofia was able to generalize and apply concepts to new objects in the same category. By reversing word order and thereby changing the acoustics of compound requests, the researchers were able to rule out the possibility that Sofia was performing based on memorizing the sound properties of requests rather than actually understanding the individual words comprising the requests.

So, you were right all along – your dog really does understand you. The problem is everyone else.

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ResearchBlogging.orgPilley, J., & Reid, A. (2011). Border collie comprehends object names as verbal referents Behavioural Processes, 86 (2), 184-195 DOI: 10.1016/j.beproc.2010.11.007.

Ramos, D., & Ades, C. (2012). Two-Item Sentence Comprehension by a Dog (Canis familiaris) PLoS ONE, 7 (2) DOI: 10.1371/journal.pone.0029689.

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Show Me the Honey! Honeyguides and Humans Team Up at Dinnertime

Humans have a long history of spotting superior abilities in other animals, and then training those animals to use those abilities to advance our own interests. Everyone’s familiar with how we’ve trained pigs to sniff out truffles for us with their sensitive snouts and how we’ve domesticated dogs to herd our livestock, alert us to intruders, guide us when our vision fails, and perform other services. Similar but less well-known examples include our training bees to detect the odor of explosives, cormorants to catch fish for us, and llamas to guard our sheep from coyotes and other predators.

It’s far less common, though, to find relationships where non-humans participate on a more equal footing, where they appear to train us at least as much as we train them. (People who are owned by cats should feel free to rebut this statement in the comment section below.)

Today’s post features one such relationship, the partnership between humans and the greater honeyguide (Indicator indicator), a bird that lives in the trees of sub-Saharan Africa.

Honeyguides and humans have very complementary appetites. Honeyguides get most of their food from beehives, feasting on larvae and wax that they extract from honeycombs (yes, they actually eat and can digest the wax!). Of course humans, too, seek out beehives, although our interest lies more in the bees’ sweet honey, and we’re generally more than happy to leave the wax and grubs for others to enjoy.

The bee-related skills of humans and honeyguides are relatively complementary as well. Honeyguides can fly swiftly across large areas and are expert at locating bee colonies, but have difficulty in extricating the combs on their own. Humans move more slowly along the ground and aren’t so adept at finding colonies, but once we have one in our sights, we’re able to overcome bee defenses and dig the combs out, even when the bees have nested deep within rock crevices and other hard-to-reach locations.

Out of this opportunity for mutualistic benefit, honeyguides and humans have worked out an elaborate interspecies communication system that allows them to work in tandem with certain signals understood by both parties.  This partnership has been formally documented in a three year field study conducted in the dry bush country of northern Kenya, focusing on the interactions between honeyguides and the nomadic Boran people who populate the area.

I’m the *real* Greater Honeyguide – don’t let imposters lead you astray! Visit me at http://safari-ecology.blogspot.com/ and see first comment below.

Each partner knows how to get the other’s attention. To attract the birds, the Borans call them with a penetrating whistle (known in the Boran language as Fuulido) that can be heard over a distances of greater than a kilometer and that is made by blowing air into clasped fists, modified snail shells, or hollowed-out palm nuts. Comparably, hungry honeyguides flag down humans by flying up close, moving restlessly from perch to perch, and emitting a double-noted, persistent “tirr-tirr-tirr-tirr” call. (Side note: I’ve been practicing this at home, and it doesn’t seem to attract much other than odd stares and raised eyebrows.)

The joint food expedition commences when the honeyguide flies briefly out of sight and then returns to a nearby, conspicuously visible perch. When the human companion approaches this perch, the honeyguide takes off, displaying its white outer tail feathers, and flies to a new resting place a short distance away, calling loudly when it lands. The Boran partner then approaches the new perch and the bird flies off again, repeating the pattern. As the Borans work with the bird, they whistle and shout to keep the bird interested in guiding. (Again, this doesn’t seem to work too well at home.)

The researchers found that the honeyguides signal the path and distance to the bee colony in a variety of ways. First, they indicate the correct direction through their flight paths, traveling consistently in the direction of the nest and increasing their precision as they near the target. It appears that the know in advance where the nests are located, as the researchers observed the honeyguides briefly visiting nests before dawn, peering into the entrances while it was still dark and the bees were docile.

Also, the honeyguides vary their behavior depending on distance to the hive. For example, when the hive is relatively distant, the birds begin the process with a relatively long disappearance during their first flight; conversely, their first disappearance is briefer when the hive is relatively nearby. Further, the honeyguides stop more frequently and the legs between perches become shorter as they and their human followers approach the nest, especially during the last 200 meters. Finally, the honeyguides select increasingly lower perches as they close in on the colony.

Upon arrival at the destination, the honeyguides perch close to the nest and emits an “indication call.” The researchers describe the scene as follows:

This call differs from the previous guiding call in that it has a softer tone, with longer intervals between successive notes. There is also a diminished response, if any at all, to whistling and shouting by humans. After a few indication calls, the bird remains silent. When approached by the searching gatherer, it flies to another perch close by, sometimes after circling around the nest. The resulting flight path finally reveals the location of the colony to the gatherer. If the honey collector does not (or pretends not to) detect the nest, the bird gives up after a while. It may then leave the area either silently or start a guiding session to another colony. In the latter case, it switches from the indication call to the guiding call and resumes a fairly direct flight pattern. Once the human team members find the nest, it becomes their turn to go to work and hold up their part of the bargain. After using smoky fires to reduce the bees’ aggression, the Boran honey gatherers use tools or their hands to remove the honey comb, and then break off pieces to be shared with their honeyguide partners.

To sum things up, here’s a great BBC video (featuring David Attenborough!) that describes the bird-human partnership and shows the honeyguides in action:

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ResearchBlogging.org
Isack, H., & Reyer, H. (1989). Honeyguides and Honey Gatherers: Interspecific Communication in a Symbiotic Relationship Science, 243 (4896), 1343-1346 DOI: 10.1126/science.243.4896.1343.

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.

Does Berlitz Offer a Course in Prairie Dog?

Yes, that’s right – before your next trip to Arizona you may need to learn another language if you really want to be able to communicate with the natives.

Prairie dog about to raise its hand in English class (photo credit: Northern Arizona University/Con Slobodchikoff)

Professor Con Slobodchikoff of Northern Arizona University has been studying Gunnison’s prairie dogs for the last three decades, and, as reported by BBC News1, believes that these social rodents have some very special language abilities. Slobodchikoff told the BBC:

Prairie dogs have the most complex natural language that has been decoded so far. They have words for different predators, they have descriptive words for describing the individual features of different predators, so it’s a pretty complex language that has a lot of elements.

According to the BBC article:

The researchers found that the prairie dogs are confronted by so many predators that they have evolved different “words” to describe them all.

These words are barks and sounds that contain different numbers of rhythmic chirps and frequency modulations.

Individual prairie dogs have different tonal qualities, just as human voices differ, but different rodents use the same words to describe the same predators, allowing the alarm call to be understood by the rest of the colony.

For example, a single bark may be attuned to say “tall, skinny coyote in distance, moving rapidly towards colony”.

National Public Radio (NPR)2 recently featured Slobodchikoff’s prairie dog research as well, providing additional color about how Slobodchikoff and his students hid near prairie dog villages, used microphones to record shrill prairie dog predator warning cries (“It sounds kind of like ‘chee chee chee chee,’ “ says Slobodchikoff), and then analyzed the sounds using computer programs to parse out the differing frequencies and overtone layers of the prairie dogs’ warnings made in response to humans, dogs, coyotes, hawks and other perceived threats.

The NPR article describes how, after Slobodchikoff noticed that there were variations in the calls used to identify individual humans, he decided to perform further tests to see how specific the prairie dogs were being in describing what they saw:

He had four (human) volunteers walk through a prairie dog village, and he dressed all the humans exactly the same — except for their shirts. Each volunteer walked through the community four times: once in a blue shirt, once in a yellow, once in green and once in gray.

He found, to his delight, that the calls broke down into groups based on the color of the volunteer’s shirt. “I was astounded,” says Slobodchikoff. But what astounded him even more, was that further analysis revealed that the calls also clustered based on other characteristics, like the height of the human. “Essentially they were saying, ‘Here comes the tall human in the blue,’ versus, ‘Here comes the short human in the yellow,’ “says Slobodchikoff.

Amazingly, it doesn’t stop there. Slobodchikoff’s next move was to see if prairie dogs could differentiate between abstract shapes. So he and his students built two wooden towers on each side of a prairie dog village. They then made cardboard cutouts of circles, squares and triangles and ran them out along a wire strung between the two towers, so the shapes sort of floated through the village about three feet from the ground. And the prairie dogs, Slobodchikoff found, were able to tell the difference between the triangle and the circle, but, alas, they made no mention of the difference between the square and the circle.

Prairie dog warning system: "One if by land, two if by sea" (photo credit: U.S. Fish & Wildlife Service)

As the BBC puts it, if Slobodchikoff’s conclusions are correct, it would mean that “the chattering rodents communicate in a more complex way than even monkeys or dolphins.”

Pretty impressive stuff.

What do you think, does prairie dog communication amount to speaking a “language”? Is human language unique in some fundamental sense, or is there a continuum between what the prairie dogs are telling each other and what we talk about among ourselves?

We will have future posts regarding animal communication and linguistic abilities, and further explore the nature of language.  Until next time, chee chee chee chee, and to all a good night!

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1BBC News, “Burrowing US prairie dogs use complex language,” February 2, 2010.

2NPR, “New Language Discovered: Prairiedogese,” January 20, 2011.

Spotted Hyenas: Clever Carnivores, Not Simply Comedians

Underestimated by many, spotted hyenas (Crocuta crocuta) are providing insight into the roots of human intelligence.

Far from being clownish buffoons, spotted hyenas – also known as laughing hyenas – live in large, complex matriarchal communities, or clans, in which social intelligence is critical. They are fascinating animals – although they look something like dogs, they are more closely related to cats, and closer still to mongooses and civets. Female spotted hyenas are the true clan leaders: they are larger and more aggressive than males, socially dominant, and have even evolved to have male-like external features, including a pseudopenis that is extremely similar in appearance to the male’s sexual organ.

Spotted hyenas enjoying the water (photo credit: K. Holekamp)

Kay Holekamp, a professor of zoology at Michigan State University, has been studying these gregarious carnivores for many years, and is particularly focused on how they can help us gain a better understanding of why certain animals, including humans and other primates, have developed high intelligence and large brains (which, from a metabolic standpoint, are extremely expensive to maintain). More specifically, she has been looking at spotted hyena society as a means of probing the “social complexity” theory of intelligence, which posits that brainpower provides a significant edge to animals living in complex social groups, where individuals need to be able to anticipate, respond to and manipulate the social behavior of other group members.

The majority of intelligence research in this area has been performed on primates, but Holekamp notes in recent research1 that social complexity theory predicts that “if indeed the large brains and great intelligence found in primates evolved in response to selection pressures associated with life in complex societies, then cognitive abilities and nervous systems with primate-like attributes should have evolved convergently in non-primate mammals living in large, elaborate societies in which individual fitness is strongly influenced by social dexterity.”

In this research, Holekamp acknowledges that much remains to be learned about social cognition in spotted hyenas, but concludes:

Work to date on spotted hyenas has shown that they live in social groups just as large and complex as those of cercopithecine primates [AW: a subfamily of Old World monkeys], that they experience an extended early period of intensive learning about their social worlds like primates, that the demand for social dexterity during competitive and cooperative interactions is no less intense than it is in primates, and that hyenas appear to be capable of many of the same feats of social recognition and cognition as are primates.

While the paper includes much more detail, the following are among Holekamp’s observations regarding spotted hyena social knowledge and skills:

  • Individual recognition. Spotted hyenas possess a rich repertoire of visual, acoustic and olfactory signals, which other hyenas can use to discriminate clan members from alien hyenas, to recognize the other members of their social units as individuals and to obtain information about signalers’ affect and current circumstances.
  • Kin recognition.Hyenas can distinguish vocalizations of kin from those of non-kin, with intensity of responses increasing with degree of relatedness between vocalizing and listening animals, and kin recognition potentially occurring among hyenas as distantly related as great-aunts and cousins.

    Basking spotted hyena cub (photo credit: K. Holekamp)

  • Imitation and behavior coordination. Although hyenas have not been observed to engage in true imitation (that is, replicating a novel act performed by a species member) the way some primates do, they do appear to modify their behavior after observing goal-directed behavior of other hyenas. In addition, they engage in cooperative hunting involving complex coordination and division of labor among hunters. This cooperation, which enables them to capture prey many times their size, involves – at a minimum – communicating by simple rules of thumb (e.g., “move as necessary to keep the prey between you and another hunter”), if not the operation of higher mental processes.
  • Social rank and social memory. Spotted hyenas are intensely aware of social rank, and they learn quickly where they and their relatives fit into their clan’s dominance hierarchy. They are able to remember previous interactions they have had with other individuals, and appear to remember the identities and ranks of their clan mates throughout their lives. They apply their knowledge of social ranks in many ways, including to avoid conflict, figure out feeding priority, help them choose appropriate mates, determine which social relationships are desirable to establish and maintain, and when to reconcile after conflicts have occurred.
  • Flexible problem-solving. Similar to certain primates, it appears that spotted hyenas are able to achieve short-term goals through a variety of different tactics. As stated in the Holekamp’s research article, “For example, a hyena can avoid aggression by leaving the aggressor’s subgroup, exhibiting appeasement behavior or distracting the aggressor. A hyena can potentially use greeting ceremonies to reconcile fights, reintroduce itself to conspecifics [AW: members of their own species] from which it has been separated, or increase conspecifics’ arousal levels in preparation for a border patrol or group hunt.”
  • Tactical deception. One sign of social cleverness, which should be familiar to all humans, is tactical deception. It appears that hyenas may share this sophisticated behavior as well, as anecdotal accounts of hyena deception include a low-ranking hyena noticing an unprotected meal but ignoring it until higher-ranking group mates were out of range, and other low-ranking individuals similarly emit alarm vocalizations in what appear to be deceptive attempts to gain access to food.

Finally, here’s a brief video in which Holekamp shows one of the ways she and her colleagues have been assessing the puzzle-solving skills and memories of spotted hyenas:

So, hats off to laughing hyenas: they may sound comical, but they are seriously smart!

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1Holekamp, K., Sakai, S., & Lundrigan, B. (2007). Social intelligence in the spotted hyena (Crocuta crocuta) Philosophical Transactions of the Royal Society B: Biological Sciences, 362 (1480), 523-538 DOI: 10.1098/rstb.2006.1993.

Fishing Buddies

We are all familiar with talented sports teams that underachieve because, despite the individual abilities of their players, they’ve been unable to “pull together” and coordinate their efforts effectively. Because teamwork requires cooperation, communication, and complex social interaction, we typically bring in outside coaches to create an environment that allows teamwork to develop, and we reserve our highest praise (and compensation) for those rare players who have the gift of making others better while being successful themselves (just ask Magic Johnson and Larry Bird).

With that in mind, you may be surprised to learn that a couple of the world’s most accomplished team players can be found not on the playing field or in the arena, but under the sea, and that they are members of different species of fish.

Grouper (from Wikipedia; photo credit: Jon Hanson)

In recent research published in PLoS Biology1, scientists reported on a highly coordinated and communicative hunting partnership between the grouper and the giant moray eel, which they observed in the coral reefs of the Red Sea. Together, the two fish make an extremely complementary and formidable hunting team.

Groupers, large predatory reef fish, are daytime hunters, while morays usually hunt at nght and rest in crevices during the day. Groupers typically hunt in open water near reefs and have trouble catching fish that hide in the holes and crevices that they find in the coral. Moray eels, on the other hand, sneak around reef crevices and attempt corner prey in holes, but have trouble catching fish in open water.

Giant Moray Eel (from Wikipedia; photo credit: Albert Kok)

As the research report observed: “The hunting strategies of the two predators are therefore complementary, and a coordinated hunt between individuals of the two species confronts prey with a multipredator attack that is difficult to avoid; prey are not safe in open water because of the grouper hunting strategy but cannot hide in crevices because of the moray’s mode of attack.”

The researchers found that hungry groupers would actively seek out their moray eel fishing partners in their crevices and shake their heads rapidly right in the eels’ faces to let them know that it was time to go for a hunt. Here’s a video of a grouper letting an eel know that it is time to eat.

The morays would then leave their hiding holes and swim off in search of food with the groupers. Here’s a video of the hunting twosome happily swimming off together for dinner.

Moreover, the pair would cooperate as they hunted. In some cases, for instance, a grouper would remain directly above a crevice where prey was hiding, perform “headstands” and shake its head to guide the moray eel to the hidden prey’s location.

The researchers noted that, when the two fish worked together as a team, the groupers caught five times as many fish as they did separately, and the moray eels caught almost twice as many fish as the groupers. (Because the morays normally hunt at night, the researchers didn’t observe them catching any fish separately, so they were not able to draw any conclusions regarding how their partnership with the groupers changed their hunting efficiency.)

This type of inter-species coordinated hunting with differentiated roles is extremely rare and had never been seen before in fish. If you think about it, this is pretty complex and advanced behavior, as the individuals must perform specific actions and play specific roles, knowing that their counterparts are doing the same. The groupers, with their intentional signaling to call their moray partners to the hunt and to direct them to prey, demonstrate particularly sophisticated, cognitively advanced behavior.

So, forget about your local sports franchise; if you want to see some especially impressive teamwork, you should put on your wetsuit and let some reef fish show you how it’s done.

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1Bshary R, Hohner A, Ait-el-Djoudi K, Fricke H. Interspecific Communicative and Coordinated Hunting between Groupers and Giant Moray Eels in the Red Sea. PLoS Biol 2006 4(12): e431. doi:10.1371/journal.pbio.0040431.

My Border Collie Is Smarter Than Your Honor Student

Or so the bumper sticker says.

On this Fourth of July, it seems appropriate to salute man’s best friend in a brief holiday post. Meet Chaser, a true canine linguistic champion.

Chaser understands more than 1,000 words, along with simple sentences. Her vocabulary includes the names of 1,022 objects, including 800 stuffed animals, 116 balls and 26 “Frisbees,” any of which she can fetch on command.

Chaser, resting after studying for the bar exam (photo credit: ABCNEWS.com)

In addition, if a new toy is placed among her playthings, she is able to retrieve it when given its unfamiliar name, inferring its identity by a process of exclusion. She also has been studying her verbs, demonstrating that she knows how to “find,” “nose” and “paw” each of her toys. I assume that next she will be working on her gerunds and finishing her mastery of the subjunctive mood.

Happy Fourth, Chaser!

You can read more about Chaser and see her in action in this ABC News1 story.

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1ABC News, “World’s Smartest Dog? Meet a Border Collie Whose Memory Astounds,” February 9, 2011.

The Awesome Octopus

I wanted to devote today’s post to a wonderful presentation on cephalopods that Maggie Koerth-Baker, the Science Editor at BoingBoing.net, gave last January at the University of New Mexico’s annual conference on Integrating Nanotechnology with Cell Biology and Neuroscience.

There is also a 10-minute edited version of the presentation, which you can find here, but I highly recommend spending half an hour to take in the full video (below), since many of the really fascinating stories have been edited out of the shorter version.

There are parts of Koerth-Baker’s presentation that I just love, particularly how she addresses the question of how we define intelligence.  As she puts it (and this part isn’t contained in the edited version):

Intelligence is a loaded word.  What does intelligence mean to you? IQ tests, grade point average, the ability to communicate via spoken language?

One thing is certain: “intelligence” makes us think of human stuff, people things. And that’s not fair.

An octopus doesn’t need to be able to pass a written exam. It never has. To judge animals against human ideas of what intelligence means in humans is to miss the point of evolution. Our brains are not this private club that the rest of animal-kind is trying to be cool enough to get into. Every species has adapted over millions of years to have a brain that allows it to be smart for its particular niche.

Octopus brains can get octopus jobs done, and they don’t have to worry about whether they can tackle human issues. Your octopus will not do your homework, but that doesn’t mean it’s stupid.

Later, she adds:

It is absolutely true that there is something very different, and very exciting, going on in the cephalopod brain, especially when you consider its nearest relatives. Cephalopods are closely related to mollusks, and their family reunion would feature such dignitaries as snails and oysters.

A layman might go ahead and call it “intelligence.” I’m just going to call it “being awesome.”

These are not big brained creatures. They can’t navigate a maze like a cephalopod can. They can’t react quickly and change their behavior to reflect minute by minute changes in their environment. And, with a couple of notable exceptions, they don’t seem to be able to remember information and use it in the future.

In the nature and in the lab, invertebrate cephalopods act more like vertebrates. Researchers describe this special class of conduct as “behavior plasticity” or “behavioral flexibility.” A layman might go ahead and call it “intelligence.” I’m just going to call it “being awesome.”

The full presentation goes on to illustrate various “awesome” abilities of the cephalopods, including decision-making, arguable tool use, and communication with other cephalopods. Koerth-Baker also provides a vivid example of how an octopus will engage in highly sophisticated mental processes in executing tactics to escape predators. When faced by a researcher perceived to be attacking:

an octopus would swim backwards away from [the researcher] toward handy places where it could hide. When it got to one of these spots, the octopus would squirt out a jet of ink in one direction, and dive away in the opposite direction, immediately changing its camouflage to match its new hidey-hole. Basically, it was giving him the old dodge and feint routine.

Now, think about everything an octopus had to do to process that. While swimming for its life, it had to know where [the researcher] was and where the next hidey holes were. It had to think about the timing to trick [the researcher] with the ink squirt. And it had to know what color and texture to turn its skin as it dove away. All of that pretty much at the same time. That’s broad awareness and complex decision-making, done at high speeds by a creature with a mollusk brain.

Verdict: awesome.

Indeed.

It really is thought provoking to consider the concept of intelligence, particularly in animals that are so different than we are. The latter part of the video provides an overview of the octopus brain and neural anatomy – if you think you know how a brain generally looks and functions (or should look and function), you will find this segment to be eye opening.

So, how intelligent are the cephalopods? They can’t read or write, they can’t speak, they aren’t particularly social. Their brains, while larger than any other invertebrate’s (and comparable in size to the brains of dogs and cats), are nowhere near the size of human brains, and cephalopods don’t exhibit many of the higher cognitive functions that we test when we measure human intelligence. Their SAT scores would undoubtedly be unimpressive.

On the other hand, how would we humans do on an octopus intelligence test, one that required us to consciously change our shapes, colors, textures and brightness in order to adapt to threats and changing environmental conditions? Cephalopods have incredible mental abilities that we are totally lacking – what does this say about whether those mental abilities are, or are not, evidence of intelligence?

These are hard questions, but one point should be pretty clear. Octopuses are awesome.

Thank you, Maggie.

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