cc  >> Clint Sprott: I'd like  to welcome you to the Chaos  and Complex Systems Seminar.  I'm Clint Sprott and this  seminar has been going on for  some 16 years, held every  Tuesday noon right here  in Chamberlin Hall.  And I'd like to encourage you to  come to other seminars in the  series.  Today we're honored to have with  us Chuck Snowdon from the  Department of Psychology.  Who is the former chairman of  that department and is the chair  of the Letters and Science  Honors Committee.  And he has interest in breeding  of monkeys and their social  learning and response to music,  and he's going to tell us about  that today.  Chuck.  >> Chuck Snowdon: Thank you,  very much, for the invitation  to be here to today.  One of the things that I want  to talk about is, I've been here  before and I've talked about  the breeding system of the  monkeys that I study, cotton top  tamarins, and some of the  interesting things that result  with respect to parental care  and their reproduction.  What I want to do today is to  focus on a different aspect of  the research I've been doing  with them over the past 30 some  years. 

 I want to, first of all, mention  that the cotton top tamarin  colony has closed so I'm talking  about work that's been done in  the past.  And there's some really exciting  work that I'll get to at the end  of the talk today, but as a good  rhetorician, I'm going to build  slowly and get to the fun stuff  at the very end of the talk.  I want to talk about  communication, social learning,  and response to species typical  music in cooperatively breeding  monkeys.  So here's an outline of the  talk.  I want to say something a little  bit at the beginning about the  biology of cooperative breeding  because it's something that most  of us don't know about with  respect to how primates organize  their lives.  I want to talk then about how  communication signals can  facilitate social learning  because one of the points I want  to make today is that tamarins  and marmosets, cooperatively  breeding primates, are  actually better at some aspects  of social learning than much  phylogenetically closer species  to human beings such as  chimpanzees and capuchin  monkeys.  And I think part of the argument  I want to make is that this is  due to complex communication  systems and a group of animals  that are very attentive to each  other's signals and each other's  behaviors when they interact.  So I'm going to talk about  avoiding noxious foods,  assisting infants to feed  independently, assisting  juveniles to learn a novel  foraging task, and also how  communication actually  interferes with donation  behavior in adults.  And finally, the third part of  the talk is to talk about some  work I've done in collaboration  with David Teie.  David Teie is a musician. 

 He plays cello for the National  Symphony Orchestra.  He's also a composer and his  work was featured on NPR last  week, one of his cello  compositions.  And David wrote me out of the  blue about three years ago  saying that he had some  theoretical ideas about music  and music's effects on emotions.  And he wanted to test these  theoretical ideas, but of course  we can't do it in humans because  all of us have been exposed to  all sorts of different types of  music, have already developed  preferences and aversions to  music, and so we need a species  that has never been exposed to  music.  That led to some interesting  problems and some really  interesting outcomes.  So that's where I want to head  today.  Let me, first of all, talk about  cooperative breeding.  Cooperative breeding is a  breeding system where fathers,  older siblings, and unrelated  individuals work together  to take care of infants.  Mothers, in fact, do relatively  little direct infant care  other than nursing.  There's limited reproduction. 

 Typically only one female  at a time is able to breed.  And the rest of the family  spends their life working  together to help that one female  successfully rear her offspring.  Helpers turn out to be essential  for survival, as I'll show you  in a minute.  And this is an unusual  breeding system for primates.  Tamarins and marmosets, which  are small monkeys from  South America, are the only  species of non-human primates  that show this behavior.  However, anthropologists have  recently argued that humans are  also cooperatively breeding  species.  That the work of rearing a child  is too much for any one  individual to do alone, and so  we humans need help in order  to rear our offspring.  So in a sense looking at  tamarins and marmosets helps us  look at species that are  different from us but share much  of the same social system and  social structure that we humans  share.  The species I want to talk to  you about are cotton top  tamarins, Saguinus Oedipus, and  the Oedipus is something that I  used to say had to do with the  fact that, we all remember from  our high school Greek classes  when we read Oedipus Rex, that  Oedipus had a club foot, and  these guys have feet that are  relatively bigger than you would  expect for their body size.  However, one of my recent PhD  students discovered that the  other aspect of the word Oedipus  also applies to these animals. 

 Young males are also known to  hit on their mothers,  unsuccessfully so far, but they  do hit or on their mothers.  So both meanings of the sense  Oedipus are covered by these  guys.  They're native to South America.  They're, in fact, only found in  a small region of Columbia.  And a recent manuscript I read  suggests that there are fewer  than 2,000 of them left in the  wild.  So much of what we're doing  throughout my career working  with these animals was trying to  figure out how to keep them  breeding and successfully alive  in captivity.  And if they're going to go  extinct in the wild, which they  could easily do very quickly, we  also want to know as much about  their behavior and their biology  as we can through studies in  captivity in order to maintain  them into the future.  They're relatively small in body  size, a little bit over a pound.  They live in trees where they  eat fruits, insects, lizards and  gum.  One of my students was studying  these animals in the wild and  her husband was studying  lizards' behavior, and one day  we had a marital crisis on our  hands when one of her monkeys  was stalking on of his lizards. 

 [LAUGHTER]  Mothers give birth to twins,  and that's an important part  about the reproductive biology.  And the twins together weigh  about 20% of the mother at  birth.  So if we take a typical woman at  130 pounds, this would be the  equivalent to giving birth to  two 13-pound babies, and females  get pregnant within two to  six weeks after giving birth.  So they're reproductively and  energetically busy providing  milk for these heavy babies and  conceiving starting another  litter.  And, smart as these guys are,  they've never figured out how to  build nests like birds do.  So someone has to carry the  animals around all day long, and  animals will travel up to two  and a half kilometers over the  course of a day in vertical and  horizontal space foraging for  food.  And so with constant caring of  infants we can imagine how it  might be very difficult for a  single mother to be able to care  for these infants by herself.  And we have multiple caregivers  needed for infant survival.  Family members are involved in  coordinating infant care,  finding food and also predator  defense.  And they have a very  well-developed communication  system. 

 We have documented 38 different  types of vocalizations or  sequences of vocalizations  the animals produce.  And this is the largest vocal  repertoire of any non-human  primate species.  So they have a very  well-developed vocal  communication system, and also a  very well-developed and  sophisticated chemical  communication system.  So what I want to ask today as a  general question is, does this  complex communication affect  their ability to learn socially?  Let me make clear the point  about how it takes a family to  rear an infant successfully.  The green bars show the survival  rate of animals in the wild when  we did a field study in Colombia  based on the number of helpers  that are present in a group in  addition to the mother.  We have a mother and father  here.  Mother and father and one  offspring, mother and father and  three other helpers here.  And notice we don't get to 100%  survival in the field until we  have family sizes of five  individuals working to take care  of infants.  Came back after having done the  field work and decided to look  more closely at the data from  our laboratory colony which we  have data on for over a 30-year  period, and much to my surprise  we found the same phenomenon  occurring in captivity.  So the yellow bars, or the not  quite yellow as they are on my  screen, kind of chartreuse bars  here, are representing captive  data, and you can see that we  don't get to 100% infant  survival in captivity until we  have family sizes that are that  large as well. 

 And this is a really striking  finding because in captivity  they're given all the food they  can eat, they don't have to  travel two and a half kilometers  every day to find food.  There are no predators to deal  with.  We keep them at a constant  temperature.  So it's an interesting puzzle to  think about why are helpers so  critical even for survival in  captivity.  But it just illustrates the  importance of helpers.  Helpers matter.  They are a life and death matter  for the survival of infants  in this species.  >> It looks like you could have  too many helpers.  >> You could have too many  helpers.  And what happens, at least,  sorry, wrong button. 

 What happens when we get out to  too many helpers is that we  usually have fights occurring in  the family.  So we have a paper we wrote  called "Family Feuds," and when  there are too many animals  around they compete with each  other over who gets to take care  of the kids and they break up  into really severe fights.  So we usually would limit group  size in captivity to about eight  animals.  And you can see that we never  found groups bigger than seven  in the wild.  So that's what we have there.  Okay, so--  I'm going the wrong direction.  So one of the things that  animals do is carry infants.  Every time I show this picture  to a naive group, you're not  naive, obviously, people say,  oh, look at the mother carrying  her baby.  And it's almost always wrong,  because you would never see a  mother carrying a baby on her  back, at best you'd see a mother  carrying a baby holding on to  her nipples, nursing, but you  wouldn't see a baby riding on  the back.  This is province of, typically,  older brothers and fathers to  take care of infants. 

 They're also involved in food  sharing.  So as females get ready to wean  infants, the weaning process is  facilitated by the fact that  adult males, typically, will  offer food to infants, and I'll  show you more about that in a  minute, they'll share food with  infants and infants become very  competent and avoid nursing and  become very quickly active in  being able to feed on their own.  So let me now look at the role  of communication in social  learning.  I argued that they have a lot of  vocal skills.  Are these important in helping  them to acquire some social  learning skills?  So I want to argue primarily  that in cooperatively breeding  monkeys, communication signals  play a very important role in  their ability to learn socially  from each other.  And the first example I want to  talk about is avoiding noxious  foods.  And lots of studies have shown  that birds and rodents very  quickly learn to avoid aversive  foods.  But there's very little evidence  that non-human primates  have this capacity.  Yet you'd think learning  socially to avoid something  that's noxious or toxic would  have very high adaptive value.  And yet study after study has  shown that primates have to  learn about aversive foods  by themselves as individuals,  not by socially interacting  with others. 

 A model study is the one done by  Elisabetta Visalberghi  and Elsa Addessi in Rome.  And they used, what we might  expect in Rome, mozzarella  cheese that they laced with  white pepper at a ratio of 16:1,  cheese to pepper.  They gave it to capuchin monkeys  which are considered to be the  most intelligent of new world  primates.  And what they found is that  capuchin monkeys fed mozzarella  laced with pepper showed  no ability to learn  from watching anybody else.  They had to learn to avoid the  pepper food totally on their  own.  So our question is, would  cooperative breeders be more  successful with this?  So we presented eight families  with highly preferred familiar  foods.  Peaches and tuna fish, which  both are eaten at 100% rate  before the study began.  We then mixed the tuna fish  in a 40:1 ratio, much lower  ratio of pepper to food  than what Visalberghi  and Addessi did.  And we then tested both foods  once a week for three weeks,  the adulterated pepper and  then the peaches in alternation,  and after three weeks were over,  we presented normal tuna  back again.  We took the pepper out because  we wanted to see what would  happen to animals after they had  this experience. 

 Is this going to have any  lasting effects on them?  So let me, first of all,  show you what happened.  Before the experiment began, 44  out of 44 animals ate tuna fish.  And throughout the experiment,  44 out of 44 animals ate peaches  whenever we presented it to  them.  But, notice when the tuna was  first presented with pepper, we  have only about 14 animals ever  sampling the peppered tuna.  So two-thirds of the animals are  avoiding the peppered tuna  without ever sampling it  themselves.  So we have some clear evidence  of social learning to avoid the  tuna.  What's also interesting is that  three weeks after this  conditioning run, we presented  the animals again with tuna fish  that was not adulterated  anymore.  And we still have a significant  number of animals or a good  proportion of animals that never  sampled tuna again throughout  the period that we tested the  animals.  And, in fact, some individuals  who had never ever experienced  tuna fish laced with pepper,  never ate tuna fish again.  So they lost access to a major  resource. 

 So there's something really  powerful about the social  learning that occurred.  Question is, what's different  between tamarins and capuchin  monkeys, or what's different  between tamarins and everyone  else who's been studied, that  makes them able to learn  socially?  And I think one of the issues  is communication.  One of the things that happened  was that animals, when they find  a food that's very palatable,  they give lots and lots of food  calls.  So animals will vocalize  with very high pitched  short vocalizations.  [IMITATING MONKEY CALL]  When they discover food.  And you can see that before and  after being presented with  peaches, there's a great  increase in the number of these  food vocalizations given.  When tuna plus pepper was given  there was no increase in the  rate of vocalizations to food  that was given.  And when tuna was presented  alone in the subsequent three  weeks after the first  presentation, again we don't  have the restoration of normal  production of food vocalizations  when animals are presented with  this highly palatable food.  So first thing that's happening  is they're eliminating the food  vocalizations that typically  attract other animals to a  source of food.  Secondly, and very surprising to  us, they started given alarm  calls. 

 These are alarm calls that they  would give in the wild  to a predator: a hawk, an eagle,  a snake.  They're the alarm calls that  they give to a veterinarian in  captivity, but here they are now  applying them in a completely  novel context.  They'd never been presented with  tuna plus pepper before, and in  this context we see a high  increase in the average number  of alarm calls that are given  per family when they're exposed  to tuna plus pepper for the  first time.  And they're still a marginally  increased rate here when normal  tuna is presented again, and  there's no change within respect  to when they're being fed  peaches.  So alarm calls are another  signal that's occurring.  And the final signal that's  occurring is a lot of facial  expressions of disgust.  So when animals are presented,  as you might imagine yourself  presented with something you  dislike, you stick out your  tongue, you wipe your mouth  against something.  They do the same thing.  They wretch and show all sorts  of signals of disgust.  And we found a lot of that  occurring in those animals,  especially who had tasted the  food. 

 So we find that tamarins are  able to learn socially to avoid  a noxious food.  Only a third of the animals who  ever sampled the peppered tuna,  and for some who never sampled  the tuna, this aversion lasted  for months and actually even for  years.  And tamarins, in contrast to the  capuchin monkeys that have been  tested in an almost and  identical paradigm, showed a  bunch of signals.  Reduction of food calls,  increased number of alarm calls,  facial reactions of disgust.  And I think these are serving to  the communicate the disgust or  the displeasure they have with  the food to other family  members, and other family  members are paying close  attention to this.  Interestingly, when I  interrogated Visalberghi and  Addessi, they said they never  heard any vocalizations from  their capuchin monkeys, never  saw any signs of facial disgust.  So there's nothing being  communicated by the monkeys to  provide a source of information  for other animals to avoid the  food.  So one of the differences is  clearly the increased number of  communication signals that the  tamarins show.  Another example I want to talk  about is how do infants learn to  feed independently.  And I alluded to this earlier  that adults are involved in food  sharing with infants. 

 Sometimes infants can even reach  into the adults mouth and pull  food out.  Tamarins engage in food  transfers with infants.  What's the role of  communication?  And does communication  facilitate food transfer?  And then do these food transfers  affect the transition to infants  becoming independent feeders?  So we presented novel food, food  that's novel to the infants,  highly preferred food, kiwi  fruit, peaches, and things like  this sort, to infants weekly for  four to 20 weeks of life.  And let me tell you a bit more  about what happened.  I said already that adults give  a food vocalization.  This is a sound spectrogram with  kilohertz on this axis and  seconds on this axis.  You see these very brief,  high frequency modulated calls  that are given when animals  discover food.  And we've shown in other studies  that animals, the rates of  calling is directly proportional  to how much they, individually,  like a particular type of food.  So animals will give lots of  calls to a highly preferred  food, very few calls to a poorly  preferred food.  But they typically give them at  fairly long internote intervals. 

 [IMITATING MONKEY CALL]  However, when infants are  present, they give a whole  series of these same note  structures.  [IMITATING MONKEY CALL]  And when they give this call,  infants come running over,  they're attracted to the adult  who's oftentimes holding food  out, literally holding food out  for them and giving these  vocalizations.  And it turns out that if we look  at animals with and without  infants, if we look at the  number of bouts of these calls  per trial, we find that they're  much more likely to occur on  trials where infants are present  than when we tested adults who  have no infants present,  and the number of total calls,  individual notes presented  per trial, is also significantly  higher when animals are  presented with a highly  preferred food with infants  present than when they're  absent.  So it's a special type of  vocalization that animals are  giving in response to having  infants present that they're  going to share food with.  And we also find that the  vocalizations are really  important if an infant is going  to be successful in getting food  from an adult.  This is the number of begging  attempts that were successful  when vocalizations were given,  and the number of attempts that  were successful when  vocalizations weren't present.  Just because the vocalizations  were given doesn't mean the  animals are always going to be  successful, but there's a much  higher probability of getting  food if the adults have called  first.  So the infants are always  begging for food once they've  learned that adults will share  food with them, but whether the  infants were actually able to  get the food transferred to them  successfully is dependent on  whether the adults are giving  these vocalizations.  So these vocalizations are  providing some sort of  permission for infants to be  able to take food from the  adults.  We find that there's a  transition that adults engage in  this vocal behavior and will  share food with infants, but it  changes over infant age. 

 So it increases from the second  to third month, but then  decreases through month five of  age.  So that the adults are  apparently reducing the  likelihood that they're going to  share food with infants as  infants get older and older.  And when they begin sharing with  food, this is looking at twins  and singletons when the first  food transfer occurs and when  they have their first  independent feed.  And you can see for both twins  and singletons there's about  a week to a two-week lag period  between when they're first fed  by an adult in the family and  when they become successful at  feeding on their own.  And you can also see that twins  are subject of food transfers  at a much earlier age  than singletons are.  And twins become independent  feeders much sooner than twins  are.  And there's a really strong  correlation between first food  transfer by an adult and when  you first feed on your own.  So this behavior of food sharing  and vocalizing has a function in  terms of helping animals make a  transition to becoming  independent feeders.  And it also has the effect of  reducing the weaning conflict  that's typical in many species  to virtually nothing because  animals are always being  supported by their parents.  >> Didn't you say that they  typically have twins though,  that the mother gives birth to  twins?  So why are there singletons?  >> Snowdon: Mothers don't always  make it giving birth to twins. 

 So sometimes there might be one  that's been resorbed in utero or  we don't exactly know, but  frequently we do have singleton  births.  So making use of that variance  that does occur.  >> So it isn't that one of the  twins was removed from the  study?  >> Snowdon: No, no.  We did nothing to intervene at  all.  And, in fact, after having spent  a long time developing a  methodology for hand-rearing  infants, we decided it was  actually too dangerous to  hand-rear infants, and we  decided that if parents are  making a decision not to take  care of an infant, we should  respect the parent's decision  and not get involved.  So this is all the natural  variation that we get, and let  me just stay with that.  So there are some parallel  studies done in the field.  Some people that I know who do  field work would never accept  something that a mere lab person  says as accurate.  So a colleague at Clemson  University, Lisa Rapaport, has  studied a related species in  Brazil, golden lion tamarins,  and she finds that she studied  juveniles and discovered that in  the wild the biggest problem  that kids faced, in terms of  getting food, is catching live  insects.  That animals can find fruit very  quickly, they don't need much  tutoring to do that, but  catching live insect prey is a  really tough skill to manage. 

 And kids almost up to a year of  age still have some difficulty  in being able to capture live  prey.  And what she finds in the wild  is that adults also gave intense  versions of their food calls but  only did it with live prey.  Although live prey are more  likely to skip out or detect  that someone is vocalizing.  So it's a kind of a paradoxical  thing, giving lots of  vocalizations when there's live  prey present, but they have a  chance to leave.  And 11 of 13 juvenile tamarins  that she studied ate the same  food on the same day as they  received a food transfer from an  adult.  And here are some results of  just calling decreases with age.  So much as I showed you before  with the captive tamarins,  lion tamarins in the wild  give a lot of calls  up from four weeks of age.  As they get older, the calling  is reduced, and once they get  about 40 weeks of age  they don't vocalize anymore.  They're not begging for food  from parents.  We also find that approaching  to an adult with food,  actual begging behavior,  and food transfers were also  systematically reduced as with  increased age across each of  these behaviors. 

 And Lisa describes several cases  of what developmental  psychologists would call  scaffolding behavior.  To give you one example,  an adult female gave a food  vocalization but had no food in  her hand.  One of her juveniles comes  scampering over and looks around  where the female is sitting and  there's a hole in the tree  trunk next to where the female  is sitting.  And the infant reaches in and  pulls out a spider that's there  and eats the spider.  So we have adults going from the  progression of having food in  their hands and offering it and  sharing it with kids directly to  this stage of where, at a later  stage, animals are being called  when they know where food is but  they don't catch it for the  infant anymore, it's up to the  infant to start catching the  food.  She has 10 examples of this that  she reports for her field study.  So adults use special food calls  only with infants.  Infants can receive food  generally only when adults give  these calls.  And adults will share high  quality foods when infants beg,  but they don't share in the  absence of infants.  And we find food sharing starts  and stops earlier with twins  than with singletons. 

 Twins probably cost more for the  family to take care of.  So they can indulge a single  infant for a longer period of  time than they can indulge  twins.  Infants appear to acquire skills  of feeding on their own.  And stop begging and feed  independently.  So they're learning to feed  out of this.  And we can talk about these  specialized adult vocalizations  as some sort of parentese.  The typical word is motherese,  but I think that's a sexist term  so I'm going to use parentese  as a more gender neutral term.  Calls specifically used with  infants to influence their  behavior.  And I'll say more about  parentese in a few minutes.  So let's move on to juveniles  and consider another task. 

 In captivity they don't have to  forage, food is sitting out in a  bowl for them most of the time.  And so we decided to created a  foraging situation analogous to  what occurs in the wild.  I wanted to see what role do  parents play as demonstrators  for juvenile learning in a  foraging task that we can do  things experimentally.  So we have a two-action foraging  device that I'll show you in a  minute.  One parent was trained with one  method and another parent with  the other method.  And then paired each parent with  one of their twins and tested  them weekly to see whether the  twins would acquire the foraging  method that the parents were  demonstrating.  So let me show you the task.  We have two opaque cylinders,  and there's food suspended  in a little dish here  that's on a string.  And one parent is trained to  come along the pole and reach up  and inside and pull the food out  from that direction.  The other parent is trained to  hang from the ceiling and pull  the string up hand-over-hand  to get the food that way. 

 And so the question is,  what happens to the infants,  the juveniles who are observing  parents, one trained with this  method, or the other parent  trained with that method?  And what we see is that the  juveniles spent more time with  the location that their parent  was modeling.  So the juveniles who had the  ceiling modeled for them, spent  more time at the ceiling than  infants that had the pole  solution model for them.  And animals who had the pole  model for them spent much more  time at the pole than did the  animals who had only been shown  how to get the food from the  ceiling.  So they're showing some  imitation of the general  location where the parents are.  And eight of the 13 animals  eventually learned to solve the  task.  And one of the striking things  that we discovered was that  there was a lot of food sharing  that went on, much as I  described for the wild tamarins,  where an adult would give a call  when it picked up the food from  the apparatus, and typically it  would run somewhere else in the  cage and share food with the  infant.  So there was infant, juveniles  would beg, they would oftentimes  get food shared with them from  the adult.  But when an animal solved the  problem at the apparatus,  the rate of refusals of parents  to give the infants further food  went up to .7.  They refused 75% of the time  after the very first trial when  their juvenile solved the task.  So very Calvinistic in my terms. 

 These monkeys are saying  the kid solved the problem once,  you don't need anymore  demonstration, I'm not going to  share with you anymore, you've  shown me that you can solve the  task, now master it on your own.  And so here we have the refusal  or the reduction of food sharing  and the reduction  of the communication signals  to indicate food sharing  as soon as infant solves  the task just once.  The kids weren't terribly good  at solving the task multiple  times so from an adaptive  perspective the parents really  were probably withholding  support from the kid  at far too young an age.  The kids really hadn't mastered  the problem yet, as I'll show  you in a minute.  So juvenile tamarins spent more  time close to the location that  was modeled.  Eight out of 13 successfully  learned the task.  Juveniles who scrounged from  their parents were less likely  to acquire the skill.  And adults with more food  transfers and more vocalizations  had less successful infants.  But parents stopped responding  to juvenile begs after the first  successful sharing.  And we have a few cases of  scaffolding, and if everything  works well, we'll see if we can  get this to show an example  of scaffolding behavior. 

 So here's an adult.  Kid's moving around.  Adult pulling it down.  Looking away.  The kid reaches up  and gets the food.  I'll show it one more time.  So you hear the food chirps  going on.  The adults reaching up.  Kid's running around.  Shows an interest. 

 Mother looks away.  Kid reaches up and takes  the food and gets it.  >> So they're almost the same  size as the adults.  >> Snowdon: Yeah.  And we've done a parallel study  with adults, and in contrast to  the juveniles we find that  adults never share food, they  never vocalize, but an adult  watching an adult demonstrator  spent very little time observing  the demonstrator and, compared  to juveniles, once the juvenile  solved the task, they were  relatively unable to go back and  solve it repeatedly.  In contrast, once an adult had  successfully solved a task,  they went back time after time.  So what we have, sorry, this  isn't where I wanted to go--  What we have in parallel here,  are three types of studies  with three different ages.  As infants, adults are sharing  foods, vocalizing, encouraging  infants to take food from them.  As juveniles, adults are no  longer sharing food with infants  until we create a difficult  situation for where they have to  learn a new foraging style, a  new foraging task, and then the  adults begin to offer food again  and share food.  But this has an inhibitory  effect on social learning  for juveniles, and we find that  adults suspend this type of  support as soon as the kids show  that they're able to solve the  task. 

 We come to adults, adults  provide no help to each other.  Even those these are long-term,  long lived mates that have been  living together, they provide no  help.  But yet the adults were able to  learn very quickly on their own.  So it's almost as though adult  tamarins are very sensitive to  the learning skills and the  knowledge skills of their kids  or of their companions and  adjust their behavior according  to the skill level of their  offspring or their mate.  Let me come up to one final  example to talk about behavior  with mates.  There's been a whole flurry of  studies recently on whether  animals have pro-social  behavior.  Are they able to share food with  others voluntarily?  And studies on chimpanzees  show that animals will not  preferentially engage in a task  where they get a piece of food  but if there's a partner sitting  next to them in a cage next to  them, the partner also gets a  piece of food.  And chimpanzees appear to be  totally unable to do this.  But chimps are highly  competitive with each other.  They're highly distractible by  food. 

 So we would argue that perhaps  cooperative breeders that share  things with each other ought to  be very different.  And a recent study on related  species, the common marmoset,  show that if you give an animal  a choice between no food for  itself and food for its mate in  the cage next to them and no  food for myself and nothing for  my partner either, that animals  will preferentially donate food  to their mate when the mate's  present.  And they are sensitive to the  presence of the mate so they  don't donate the food when  there's no one in the cage next  door.  We independently developed this  almost identical task for cotton  top tamarins and found exactly  the opposite results.  Our monkeys showed no interest  in sharing food with their  long-term mates.  Even monkeys that they'd been  living with for five to 10 years  in some cases.  There was no interest in sharing  food with them.  And this is to show the design.  We have a donation apparatus.  The animal is free ranging here. 

 Another animal is in this cage  here.  There are two trays.  One which has no food on it.  The second tray has one piece of  food that will go to the  recipient but the donor is  unable to get it, and the donor  can choose which one of these  two trays to pull.  And it appeared almost as though  the animals were acting at  random.  That is, they didn't seem to be  paying attention to whether  their partner was present in  this cage or whether the partner  was away and unable to make use  of the food kept the partner  back there.  But one really interesting and  kind of bizarre result did occur  and that's that animals were  less likely to donate food,  significantly below chance  levels, if the mate showed any  interest in the food.  [LAUGHTER]  So if my mate is in the cage  next to me and she's giving  food vocalizations,  look what happens.  She gets a lot less food  when she does.  I'm much less likely to give her  food than I am if she doesn't  make any fuss at all. 

 If she shows reaching behavior,  to try to reach at the food  that's there and shows an  interest, again we see a  significant drop in terms of  how likely I am to donate food  to her if she shows any interest  in the food at all.  Bernard.  >> Is vocalization involved  in what you just described?  >> Snowdon: The donor wasn't  vocalizing, but, in this case,  the potential recipient  is begging for food.  >> Fruitlessly.  >> Snowdon: Fruitlessly.  So these animals  simply do not tolerate whinging.  If you're going to be a good  tamarin partner to someone, you  just don't engage in whinging  behavior because it's not going  to get you anywhere.  >> Would they feed the babies?  >> Snowdon: We didn't have  babies to test at this time,  but they did do earlier,  when there were infants present  is they would share food  readily with infants.  So I think if we had this formal  apparatus set up, I think they  probably would have donated to  infants.  So, again, infants and juveniles  are privileged to some degree in  terms of this behavior compared  to adults. 

 Even someone that you've lived  with for a long period of time.  You can think about that in  terms of your own relationships.  [LAUGHTER]  So almost perversely,  donation rates to partners were  even lower when the partner  gives food calls or shows some  interest in the food.  Thus, food calls and reaching  actually inhibit donation  behavior.  So we've talked about tamarins  performing better on some social  learning tasks than other  primates.  They use communications signals  that both facilitate and can  also inhibit social learning and  donation.  We find alarm calls used in a  totally novel context when  animals are presented  with an aversive food.  And we have specialized calls of  adults when transferring food to  infants as a possible form of  parentese.  And this suggests that maybe  there's some form of teaching  that's going on if adults are  systematically scaling their  behavior toward offspring and  toward mates according to what  the knowledge of the mates  already is or infants already  is, then we could argue that  this is some form of rudimentary  teaching.  Now I want to focus more on the  musical side of things. 

 So let me stop for a second and  see if I can get this next one  up.  >> Chuck, is it true that in the  wild there's sufficient food?  >> Snowdon: There may not be in  the wild.  And why is this not loading?  § §  Well, it did work earlier.  Okay, where I was going to go  with this was to show you  a nice video that was made  by the "New York Times,"  for this next part,  where I'm going to talk about  music in tamarins is something  that was featured  in the "New York Times Ideas"  magazine in December,  and this worked earlier.  I can show it to you afterwards.  It's a nice animation that was  created to go with the website,  and I can show it to people.  Let me make the transition here.  We have lots of evidence that in  language that prosody, the  intonation contours of human  speech, can affect the behavior  of infants and companion  animals.  And Anne Fernald at Stanford  University talks about motherese  in human infants.  As I said earlier, I think we  should be gender neutral in  terms of this. 

 And Patricia McConnell, who many  of you may have heard about who  lives in Madison, found similar  structures affecting the  behavior of border collies and  other working animals.  So one of the things we wanted  to examine is will animals  produce signals with similar  features that will also change  the behavior of recipients the  way we do.  So McConnell found that looking  at people working with Scottish  border collies and sheep herding  trials was that there was a  series of features that all  shepherd dog pairs had that got  dogs aroused and active.  And it was basically like if I  were communicating with a horse.  Come on, giddy up, giddy up,  giddy up.  [CLICKS TONGUE]  A series of broad band sounds  that are very short staccato  features.  If you wanted to slow down the  dog and get it to slow down,  you use a long and typically  descending note.  Whoa, whoa.  And that has the effect of  slowing a dog down.  A very brief or a very short  frequency modulated call. 

 Stop!  No!  Turns out to be something that  inhibits movement.  And I don't want to go into all  the other parts of what she did.  She did several other things.  I can talk about it in  the question session.  But what I am struck with is how  similar the calls, the sounds  were that human adults make to  their babies across different  languages.  And this is taken from Fernald.  Nein, nein.  No, no.  [SPEAKING FOREIGN LANGUAGE]  So we have similar types  of calls, spectrograms  that look very similar to what  humans are using with their dogs  when we look at how they talk  to their babies.  For attention or getting them  to do something. 

 Can you get it?  Can you get it?  Come here.  Come.  [SPEAKING FOREIGN LANGUAGE]  So we have this upwardly rising  short notes.  And then for calming down.  Aw.  Oh, honey.  Oh, Danielle.  [SPEAKING FOREIGN LANGUAGE]  And so forth.  So we have the same vocal  prosody patterns being used with  our animals as we do with  people.  And McConnell found that this  wasn't just restricted to  shepherds and sheep dogs, it  worked with, if she looked at  shepherds and -- sheep herders,  it wasn't unique to  Indo-European languages. 

 She found that Chinese  informants were asked about how  they call their dogs or talk to  their cats, they used the same  patterns of sounds.  So it's cross-linguistic, these  patterns that are being used.  And they have clear effects on  the behavior of animals and of  our children.  So what are the implications of  this?  Well, some theories of the  evolution of music have argued  that parentese is one idea of  how music influences behavior,  and lots of people in talking  about the evolution of music  have focused on how the social  emotional role of music is  related to prosody and speech  and how music may have evolved  first as a basic way to  communicate emotional state to  one another, and we've added  that on top of our speech.  If you ask me,  "Chuck, how are you?"  And I say, (in depressed tone)  "I'm fine."  You probably don't pay attention  to the actual language that  I'm producing, you pay much more  attention to the prosodic  features.  Or if you ask me,  "Chuck, how you are?"  And I say, (in sing-song tone)  "I'm feeling crappy today!"  Again, you probably don't pay  much attention to the actual  words that I'm saying.  And, in fact, I think we do  communicate our emotional state  much more effectively through  the prosodic aspects of speech  than we do through the actual  linguistic parts of it.  So the question is, do the  emotional aspects of what we  understand as music appear  in other species and serve  similar functions?  And do animals signals have a  direct emotional influence on  the behavior of recipients?  And this is where David Teie  comes in as a collaborator.  And, as I said, he wrote me  about this theory he had on  music's effects on emotions.  So we started brainstorming  different ways to do this. 

 And one of the problems we have  is that a study had been done on  the same species already that  presented cotton top tamarins  with a choice of German  techno rock versus Mozart.  And of course we all know the  answer.  Monkeys prefer Mozart.  But then they went on and did  yet another study where they  presented the monkeys with a  choice between Mozart and  silence.  And guess who won?  Silence.  So monkeys in that study appear  to be relatively indifferent to  human music, and the conclusion  was monkeys just don't have any  appreciation for music  whatsoever.  I mean, giving up Mozart for  silence, come on.  So monkeys don't have the same  musical values that we do.  But the problem is monkeys call  at a higher frequency, up to  three octaves higher, and their  tempo is about twice as fast as  ours, and so maybe they're  indifferent simply because our  frequency range and tempos just  don't have any meaning for them.  But it could be that the same  principles of communication are  effective for both species. 

 So if we're going to look at  music that contains various  types of motive elements, we  need to think about music that's  composed in the frequency range  in tempo for monkeys, and then  test that to make sure that's  the reason, we're going to  compare animals to music  composed for humans with music  composed for tamarins.  So David and some musician  friends of his who did not know  the context of tamarin calls.  I sent them sound files and they  would sit and do a musical  analysis of it.  And this is kind of our  regression to where things were  back in the 1940s before we had  good physical equipment for  measuring acoustical features  precisely.  People would use their musical  skills and identify animal  sounds in terms of,  and write them on the score.  We found that affiliative calls  were narrow frequency bands  using head voice or falsetto.  Long notes, typically with  seconds, thirds and fourths,  major intervals.  Threat responses  were broad band, not pure tones.  They were short notes, staccato  and lots of descending thirds,  fourth, fifths, and sixths.  High fear had several short  staccato notes, and also some  dissonance, minor seconds. 

 Confident threats were  relatively long calls that had  ascending notes, again forming  nice harmonic structures in the  diatonic scale.  And things that were soliciting  approach tended to be triple  meter.  That is, a waltz time  is triple meter, or polka.  [IMITATING TRIPLE METER]  And also produce these rhythmic  triple meter things and these  typically, although they varied  in terms of their musical  features, tended to be involved  in soliciting approach.  Sir.  >> You say second, third, and  fourth, do you really mean what  humans call second, third and  fourth?  Or do you mean it's sort of  close to what we would --?  >> Snowdon: It's what  the musicians classified it as.  So I don't know exactly how to  answer.  It's what the musicians said it  was.  I don't have perfect pitch,  and I can't tell you that.  But I'm going to give you an  example, and you can identify  for yourself what you think. 

 So some general principles that  David came up with was the tonal  structures are going to be  associated with positive  interactions.  Atonal or dissonant is going to  related to aggression, fear or  defense.  Pure tones are going to be  positive, associated with  positive events.  Harsh, noisy calls  with negative events.  Staccato calls are going to be  arousing.  Longer notes are going to be  calming.  These all come very close to  some of the features I've just  been describing in parentese and  how we communicate with our  animals.  But there's some additional  variables here.  So do tamarins themselves make  music in terms of their calls?  We have some aspects where we  can identify clear tonal  centers.  One animal call, typically an  E flat major, at least according  to the musician listening to it. 

 So there seem to be some tonal  centers.  One of the early calls I sent to  David to dissect was this one.  [MONKEY CALL]  And he told me this was  a very aroused animal.  Something is making it very  fearful.  And, in fact, what was going on  was that someone was dressed in  a monkey catching uniform to go  catch monkey for veterinary  treatment and that's what we  got.  And if we transpose this down  to our hearing range.  [SLOWER, LOWER-TONE MONKEY CALL]  Still pretty noisy.  Lots of dissonance,  lots of noise.  Now, I sent him another call  that was recorded just four  minutes later.  [MONKEY CALL]  It also sounds like a squawk  and nothing much interesting  in that. 

 But let's slow that one down.  [DESCENDING PITCH MONKEY CALL]  Now, I don't know.  I'm hearing something close to  major thirds and it's the  descending sequence.  And quality here is not the best  from the speaker.  So there's something going on,  and what sounded like a squawk,  now becomes, when we slow it  down to our hearing range, is  something that has a clear tonal  pattern to it.  And this is a more relaxed  confident animal.  The guy dressed in the monkey  catching uniform wasn't going  any further, and the animals  were showing confident threats  at this stage and so we have  that.  We also have, basically, what  David would described as themes  and variations.  [MONKEY CALL]  I'll go slower.  [MONKEY CALL]  So we have very similar notes  when we put them on a score,  and structurally these would be  acoustically slightly different  from each other. 

 But we have the same animal  repeating this series of calls.  Animals also chorus with each  other.  [MONKEY CALL]  This is going to be very loud  so I apologize.  [MONKEY CALL]  Let me turn that off.  So if calls have direct  emotional effects on recipients,  then music composed to include  these components should affect  the behavior of animals.   So we decided to compose music  in the frequency range and the  tempo of tamarin calls but with  similar pitch changes and  thought they should be more  effective than similar calls  composed for humans.  We tested seven pairs of monkeys  with two sets of stimuli.  Two examples of what we call  human calming music, two sets of  tamarin calming pieces.  Two human arousing and  two tamarin arousing pieces.  And we had a five-minute  pre-stimulus baseline,  a 30-second excerpt of music,  followed by a five-minute  post-stimulus behavior  response period. 

 And for human calming music,  I was told by the people at the  Public Television, which is  videoing this, that I'm not  allowed to play the samples  of the human music, because  they would be copyrighted,  and the recording industry  would be all over us,  so I'm not going to play those.  But human calming music was  typically in the lower range of  a woman's voice.  35 to 40 notes per minute.  Pure tones and harmonics.  One of the examples was  "Barber's Adagio for Strings."  Another one was a solo piano  piece from Nine Inch Nails.  Both of which have these  characteristics.  Tamarin calming music I'll play  for you in a minute, but notice  how the frequency range is much  higher.  The rate of notes per minute  is almost twice as much.  And we have both descending  two to four note motifs  to match the repetition  of tamarin calling calls.  But in tamarin calling calls,  we also have  ascending frequencies. 

 So I'll play some examples  of that.  So here are the two examples  of tamarins.  [SHRILL, MUSICAL TAMARIN CALL]  Now if you're listening to this,  something you can ask yourself  is, tamarins don't like Mozart,  how much do you like this music?  [LAUGHTER]  This is calming them,  but it sounds like a bunch  of finger scratchings  on the blackboard to me.  And I won't go through  the whole example.  [SHRILL MUSIC CONTINUES]  Sorry, I just messed that  one up.  I have two pieces  going at the same time.  That's my bad.  Okay, that's not  what I want to do.  Maybe that will work.  Thank you. 

 >> If you shifted that down to  our range, would it sound better  to us?  >> Snowdon: It would sound  better to us at our range, yeah,  particularly the second piece  which is not shown in the score.  The other thing to bring up  is that it turns out that when  we drop things three octaves  we're in the frequency range  of the cello.  And so my collaborator  is a cellist.  So this is played on his  1748 cello from Italy.  So this is probably the most  expensive piece of scientific  equipment I've ever worked with  is to have this guy playing the  cello music.  Okay, so human arousing music we  took pieces from Metallica,  "Of Wolf and Man," another piece  called "The Grudge" by Tool.  And it goes at 80-260 Hz,  200 to 300 notes per minute  which is almost danceable.  Minor modality, lots of minor  seconds and tritones, lots of  noise added with a fuzz box.  Tamarin arousing music is,  again, much higher.  500 to 550 notes per minute. 

 Ascending crescendo motifs.  Lots of broadband  unvocalized aspirants,  so much of the fuzz box.  And lots of minor seconds.  So again I'll just play  the two examples.  [MUSICAL TAMARIN CALL]  So imagine yourself  dancing to this.  [MUSICAL TAMARIN CALL]  And the second example.  [MUSICAL TAMARIN CALL]  So what's the effect of this?  If we look at post-stimulus  behavior, after they've heard  the music, we find that looking  at the fear of threat based  music, arousing music versus the  calming music, we have a clear  difference in the amount of  movement that animals show  on average across this period.  We have a significant difference  in the amount of anxious  behavior that they demonstrate,  more to the arousing music.  And, paradoxically from our  perspective, a lot of increased  level of social behavior  relative to the other music.  And the social behavior we think  is likely to be due to the fact  that the animals are huddling  with each other and maybe  reassuring each other in the  context of this music. 

 And what's interesting is that  the music has stopped.  This is looking at the five  minutes after the music is over  and we're seeing that there's  some long lasting behavioral  effects.  We look at the calming music, we  find that, this is comparing the  baseline condition when animals  were relaxed and weren't very  active.  If we look at movement behavior,  we find that comparing the  before music to after music with  the calming music, there's a  significant reduction in  movement, reduction in  orientation and increase in  foraging behavior and social  behavior is meant to be  calming and relaxing.  Monkeys find a significant  reduction in the amount of  social behavior that they  displayed.  So we're able it induce  behavioral changes in these  monkeys, that differ from their  baseline behavior and differ in  comparison with each other,  by playing the monkey music.  We found almost no effect  of human music whatsoever.  No behavioral changes occurring  there.  With one curious exception.  Which got me lots of interviews  on rock stations around the  world when the feature was being  released because animals were  calmer when they heard  Metallica and Grudge. 

 And why is this?  Well, it turns out that if we go  back and look at the human  arousing music,  it's about 260 Hertz.  If we go back and look at what  it would be for calming music  for the monkeys--  Actually I'm not getting it.  Calming music for the monkeys  is, actually, it's not making  the point I wanted to.  200 notes per minute,  is what I wanted to get to here,  is about the resting heart rate  of the tamarin.  So what we're doing is producing  sounds with Metallica and with  Tool that are at the same  frequency rate or the same  pulse rate as the resting pulse.  So if pulse rate reflects  calmness, if resting pulse is an  indicator of calmness, then  having a tempo that matches your  resting heart rate might be  something that would be expected  to be soothing.  >> Did you try exposing them to  Mozart at twice the speed?  >> Snowdon: Haven't done that.  One of the issues is it's not  just twice the speed, it's twice  the speed, but also three times  the frequency.  So we have to do something more  subtle than that.  And one of the other differences  is that for humans and for dogs  it's descending notes that seem  to be calming. 

 For tamarins it's, again,  paradoxical that show an  increase in frequency across  calming notes.  So the two pieces of music  I've played actually combined,  one piece had the descending  motifs and the other  had ascending motifs.  We could double Mozart  and play it backwards.  [LAUGHTER]  "Paul is dead."  So we find that we have distinct  musical components in tamarin  call structure and they vary  with context.  We have dissonance in fear  situations, harmonic chord  structure and confident threats  in the affiliation.  Staccato notes are related to  increased arousal, and the major  difference between prosodic  features in humans is that we  use descending intervals for  calming and tamarins seem to use  ascending intervals.  And tamarins are relatively  indifferent to human music but  respond with behavioral changes  to music in their own frequency  range.  Sir.  >> Have you tried to decouple  the effects of rhythm and tone,  going back to Metallica?  >> Snowdon: Yeah.  >> The rhythms and monotone to  see if that has any effect?  >> Snowdon: We have not and,  unfortunately, the colony  doesn't exist anymore so I can't  go back and do that. 

 There are lots of interesting  questions we'd like to pursue.  It would have been wonderful  just to decouple the tempo.  There is a guy, about the same  time as our paper came out in  September, there's a guy who  published a paper on rhythmic  dancing, a cockatoo and showed  that if, you can look it up on  YouTube, the dancing cockatoo,  and as you change the tempo,  the cockatoo's dance rate gets  faster and faster, and it flaps  its wings and it's tapping its  foot in nice rhythm to the  tempo, and they're increasing  the tempo as time goes on.  I would love to see what happens  to the monkeys, but I don't have  that opportunity anymore.  So the emotional induction  aspects of music, may in fact  have a long evolutionary  history.  We see prosodic features in how  we communicate to our dogs, as  well as what we see in monkeys.  And some of these features are  found in differential call types  that we can find in songbirds  that are around us as well.  So this suggests that some of  these features that we use in  musical composition may have  a long evolutionary history.  Playback of music that's  composed with features of  arousing and calming signals but  not the actual calls suggest  that call structures might have  evolved not only just to  communicate what one's emotional  state is, but also maybe to  induce emotional state in  listeners.  And that's clearly what we do  when we choose music to monitor  or affect our own moods. 

 We choose different types of  genre according to the mood that  we want to induce in ourselves.  And suggests that calling,  in monkeys or in other animals,  might have, as one effect,  a listening emotional contagion  in listeners.  One final implication of all of  this is attempts to use human  music as an enriching device,  which a lot of primate labs are  doing now to try to calm their  monkeys, is probably very  misguided.  And I talked to several  reporters about this work, and  many of them would volunteer  that every morning when they  left for work they would turn on  the radio for their dog, cat,  whatever, to listen to and I  would say so what do you tune it  to?  And someone would say, my dog  really likes public radio and  classical music so I put the  public radio station on.  And someone else would say, I  put on country western because  that's what the dog really  likes.  Or someone else would say, I put  it on to soft rock station  because that's what's best.  So, basically, people are  projecting their own musical  genres, their own musical taste  into their pets, and people are  doing it right now at primate  facilities on campus where  whatever the caretakers want to  listen to as they're working  during the day, is what the  monkeys have to listen to.  And if those blackboard  scratches sounded awful to you  as I was just playing them but  sound good to the monkeys, just  imagine what it would be like to  be suffering every day to have  to listen to music that we  prefer but that not necessarily  the monkeys prefer.  So I will stop there  and take questions.  [APPLAUSE]