Wisconsin Public Television University Place Forum on Animal Research  Charles Snowdon The Cotton-Top Tamarin: Research for Conservation and Understanding Human Behavior  March 29, 2011 UP573    cc >> Robert Streiffer: I am a member of the planning committee for this series of talks, and it is my pleasure to introduce our speaker tonight, Dr. Charles Snowdon. A little bit of background and then I'll turn the floor over to him, and we should have plenty of time after his official presentation for Q&A. Professor Snowdon received his BA from Oberlin College and his PhD from the University of Pennsylvania. He taught here at UW Madison since 1969. He held an NIH Research Scientist Award for 23 years and has been awarded two named professorships here at UW, a WARF University Houses Professorship and the Hilldale Professorship. His research grant supported a colony of endangered monkeys for more than 30 years, and he is one of the few psychologists who has done extensive field work on the species that he also studies in captivity. He supervised a wide range of student projects out in the field that ranged from research on mountain gorillas in Rwanda, to chimpanzees in Tanzania to cotton-top tamarins in Colombia to pygmy marmosets in Ecuador, to common marmosets in Brazil and even southern right whales off of Argentina. Professor Snowdon served a three-year term as editor of Animal Behavior and subsequently served a six-year term as editor of the Journal of Comparative Psychology. He's been associate editor of several journals including Behavior, the International Journal of Primatology and also Advances in the Study of Behavior. He's also served on numerous editorial boards including the American Journal of Primatology, the International Journal of Primatology, Primates, and now I have to say this with a French flair, Primatologie. 

>> Primatologie, oui. >> He's edited over a dozen books including Primate Communication and Social Influences on Vocal Development. He served on the American Psychological Association's committee on animal research and ethics. And he was an invited member to the National Research Council Committee that developed the official national guidelines for psychological well-being of nonhuman primates. And he's also served as president of the Animal Behavior Society. More locally, he served as a member of the Letters and Science Animal Care and Use Committee here at UW for six years, and he chaired, in addition to that, he chaired the committee for another seven years. So a lot of local experience and national experience as well. And just before I turn the mic over to Professor Snowdon, I'd like to remind the audience that our next speaker in the series is going to be Professor Gary Varner who is a bioethicist from Texas A&M, and he's going to be discussing personhood, ethics, and the cognitive capacities of animals. And that talk will be here in this room at 7:00 PM next Monday on April 4th, and we hope you can make it. And now, without further ado, Professor Snowdon. 

[APPLAUSE] >> Charles Snowdon: Thank you very much, Rob. It's a great pleasure to be here, and I apologize that my voice is not the best. I had to lecture this afternoon. >> Sorry, could you mute the mic with the bottom button? >> Okay. Did that work? So what I'd like to do today is to tell you about some research that my colleagues and I have done with a really interesting species of cotton-top tamarin. And I want to talk about the cotton-top tamarin both from a conservation perspective and why research is important to help conserve endangered species and also to talk about some interesting aspects about cotton-tops that I think should be appealing to humans as well. So, first of all, I want you just to imagine what perceptions you have about primate research, and what I'd like to do is hopefully overcome some typical perceptions about primate research and present you with some other ways to think about primates and other ways we can be studying primates in the captivity. The species I'm going to talk about and focus on tonight and the cotton-top tamarin. It's cute in these pictures, which were taken by a colleague of mine, Carla Boe. All the captive pictures are from her. 

Their official name is Saguinus oedipus, and that's not just because they have kinky sex with their mothers, which they don't, but as you recall from reading the Oedipus myth, you probably remember that Oedipus had a club foot. And if you notice these guys, they have seemingly bigger than normal feet. They are native to Colombia, and I'll say more about their natural history in just a bit. I'll say about it now. They're natives South America, a small area of northern Colombia. They have small bodies. They weigh about 500 to 650 grams. So a pound to a pound and a half. In the wild they live in trees eating fruits, insects, lizards, and gum. One of my graduate students, her husband was studying lizards at the same site as a related species and we had marital discord one day when her marmosets were stalking and trying to eat his lizards. 

But they do eat lizards and insects in the field. Mothers give birth to twins, and this is a singular part about their biology that's really important because the twins together at birth weigh about 20% of the mother's weight. So imagine 130-pound woman giving birth to two 13-pound babies. That's the equivalent of the birth effort that mothers go through. Females can seed shortly after giving birth, four to six weeks after they give birth, and I think these guys are very smart and very intelligent and I'll talk about that later on in the talk, but I think what has surprised me about them is that they have not been smart enough to learn to build nests so that means the babies have to be carried constantly. And estimates of how far they travel in the wild or estimates about two kilometers a day, and that's two kilometers a day on the ground but, in fact, these animals are arboreal and they move up and down in the trees. So they cover quite a lot of ground and carrying two heavy infants and nursing them while you're simultaneously pregnant with your next set of kids creates some interesting biological problems for them. They're called cooperative breeders and cooperative breeding is a breeding system where fathers, older siblings, and unrelated individuals can work together to help take care of infants. Typically, cooperative breeders are characterized by limited reproduction. Only a single female, and oftentimes a single male, breeds. 

This is a relatively unusual breeding system for nonhuman primates, so it's relatively common in birds. But it is said by some biological anthropologists to be the breeding system that's typical for humans. That is, we humans cannot reproduce successfully without having help of some sort, and whether the family to raise the child, whether it's the extended family, or whether we pay for childcare, we have to have someone to provide some help along the way in order to rear infants successfully. So tamarins and marmosets, their close relatives, are possible primate models for the study of affiliation, pair bonds, and cooperative care, all of which are aspects of family life that I think these animals can tell us something about. So I want to pose some questions that I want to try to touch on today about why are cotton-top tamarins interesting. They're monogamous, at least serially monogamous the way most of us are throughout our lives. They may have multiple partners throughout their life, but at any one time, we find from studies in the field, they are only mated with a single partner. What hormones might be involved in maintaining monogamy or helping animals get together and form a close relationship? One of the interesting characteristics about cooperative breeding is that fathers and older brothers, in particular, become good infant care givers. So what's the role of learning to be a parent and how does that occur? What is the role of hormones and priming a male to become a good caretaker? How do parents keep other animals from breeding? How does a female maintain her own reproductive sovereignty and prevent other animals from breeding? And finally, a question that's occupied us in the last several years before a colony was closed, is how does cooperative breeding lead to better social learning and better corporation with others? I'll try to report some data later that I think shows some really interesting differences between our closest relatives, chimpanzees, and these cooperatively breeding tamarins which have a lot of other interesting characteristics that animals like chimpanzees do not have. But before I answer these questions, let's take a trip to northern Colombia and visit the animals in the wild and see what their habitat is like. 

I guess I want to first of all mention that I'm an accidental primatologist. I inherited the colony of monkeys that I began working with from a colleague who could no longer support them in Berkeley. So I didn't start out with the plan that I was going to study primate behavior, but I saw these animals and they caught my eye, they caught my attention, there were lots of interesting things about them that made them very exciting and very interesting to want to learn about further. So what I want to talk about next is how easy are they to study in the wild? What's their current conservation status? How many remain and how does captive breeding fit in as a way of conservation? So let me, first of all, let you take a few minute to find the cotton-top tamarin in this picture. If you were a field biologist this is actually a good time to look at these animals because it's the dry season and most of the leaves are off the trees, so, in fact, the monkeys are very visible in this time of the year. So how many of you have found the monkey? This is what it would be like if you were studying these animals in the wild. Where are the monkeys? Where are you going to find them? How are you going to identify them as individuals? Anyone find them yet? Anyone think they found it? Let's draw a circle around it so you can see it. Now if you look really closely, you can see the same sort of monkey that I showed you the close up picture of earlier. So had a field study going on at Colombia for several years, and let me show the area of Colombia where our animals are located. This is northern Colombia. 

Here's Colombia, Venezuela, Brazil, Peru, Ecuador, and we're seeing that just in a very small area of northern Colombia is where these animals are located. The two big cities on the Caribbean coast, Barranquilla and Cartagena, which have huge numbers of people living in them, over a million people each, we worked in a field site in Sincelejo for several years, about six years, and then were finally driven out by some guerillas. So one of the problems about working in Colombia is that it doesn't have the same sort of civil society that we're accustomed to in the United States. And so these orange areas, the orange outlined areas on this map, are areas that are not safe for people to visit unless you're part of the narcotraficantes or part of the guerillas who are working in Colombia. And our field site near Sincelejo is now part of this area that is no longer a place where we can go. The green areas show forest that was determined from satellite photographs in the year 2000. So just 11 years ago, the green areas represent the forest that visible then from satellites. The dark green dots, you can see scattered around here, are the forest areas that are suitable for supporting cotton-top tamarins found in 2006 and 2007. So how many of the dark green areas can you identify and where are they located? So one of the problems we face is we can't, it's hard to create a conservation area in Colombia when you have areas of civil unrest, and an area where we tried some conservation work near Sincelejo is now out of bounds to outsiders. You can see very small areas of dark green, and what this leads to is then a question we could ask is, how many monkeys are left and what is their status in the wild? Anne Savage, a former undergraduate and graduate student of mine, published a paper in Nature last year that provides some information about these animals. 

So let me, first of all, indicate that some of their habitat loss has occurred from farming. These are very recent pictures taken in Colombia in the areas where cotton-tops live. We have logging that goes on and we have wood being collected for charcoal production as an energy source for people to cook. Anne Savage making use of a technique that Patricia McConnell and I devised 25 or so years ago. We found that in captivity if animals heard the vocalizations of a stranger, they would vocalize in response to the strange calls. And what Anne Savage did was to take this technique and have teams go into the field making these transects across the areas where cotton-tops live and every 10 meters they would stop and play back the call of a strange monkey and they could keep track then to how many times did they hear answers to those calls and how many different answers did they hear? And using this they surveyed 45 patches, which they published last year, representing 27% of the area that they can get access to. And they found that there are approximately 2,045 tamarins left in this area. There's a range of error in their estimates. So this is the range that they show. And if we assume the same densities of animals living in the unsafe areas, what this leaves us with is about 7400 animals likely to be remaining in the wild. 

This contrasts with 20,000 to 30,000 that were imported into the United States in the 1950s and 1960s. But since 1970, it's been habitat destruction that has been the major cause of the decline of populations. So research related to conservation I think is critical. Reserves are not easy to create and maintain in Colombia. We can't predict when a group of guerillas or narcotraficantes is going to want to take over an area that we're trying to preserve. Captive breeding and research I think are an important supplement to conservation in field. But in order to captive breeding, we have to learn how to do it properly. We have to learn what are the parameters that are really critical for successful captive breeding. And I think it's really important that we develop noninvasive methods because what we want to do is to use methodologies that will help us understand the animals and how they can breed successfully but we don't want to do anything that's going to disrupt their natural behavior or disrupt their ability to reproduce. The same time I think anytime we work with an endangered species there's a moral imperative to learn as much about that species as we possibly can before it goes extinct. 

So rather than letting an animal die out and just say tough luck, you just picked the wrong place to live, I think it's really important that we, as biologists and psychologists and anthropologists, spend our energies trying to understand what is it that we can learn from that species that might help us, might help us understand other nonhuman primates, might help us understand how to conserve primates. So I think research plays in a very important role. Research has to be done right and has to be done carefully. So in order to start our captive breeding program, we found we had six major myths we had to overcome. And let me deal with each of these myths in return. When we first began in 1978, the idea was that good research had to be invasive, and I'll talk about some of the ways that we've dealt with coming with noninvasive ways. It was thought that a mother or a mother and father were sufficient to raise offspring. They didn't know about cooperative breeding, they didn't know about the importance of having, possible importance of having helpers to rear infants. Most of the biologists who were breeding cotton-top tamarins in captivity in the 1970s believed that parenting skills were innate. And, therefore, what they could to was to take infants or take adolescents away from their family groups at an early age and get them to breed, and I'll show you what the consequences of not letting animals stay at home and live with their parents for a period of time are. 

They're significant. Cozy cages were thought to be sufficient. And I'll say some more about cage size and cage volume. We had a big run in with our veterinarians in the 1970s because there's a belief by veterinarians that all surfaces have to be impermeable and sterilizable, and yet there's some good reasons, biologically, why not all surfaces should be that way for tamarins. Sterilization is important, cleanliness is important, but we need to think carefully about the biological needs of the animals as well. And finally, people ask a lot about should animals be reintroduced into the wild? And there's a thought among many biologists, many of my colleagues, that predator fear is something that is innate, that animals don't have to learn about predators. And I want to try to argue that these are all myths that have to be overcome in order to rear and think about reintroduce in a serious way. So, noninvasive methods can work. We developed ways to minimize handling of animals by, among other things, luring them down to stand on a scale by giving them a raisin or a treat, and they would sit on the scale and we could weigh them. We could medicate them by hiding the medication in a piece of cookie or piece of banana and feeding it to them through the cage walls so we didn't have to capture the animal every time we wanted to give it an antibiotic or give it something else. 

We figured out ways to transfer animals to new environments without having to capture them or ever handle them, through air condition ducting and I'll show you that in a minute. Also monitored hormones by collecting urine samples which is a very easy way and a very unorthodox method of looking at urine samples, of looking at hormones back when we started. And we ended up testing the cognitive skills of the animals by bringing the apparatus to the animal rather than taking the animal away and putting it somewhere where they would have to work with the apparatus in a strange environment. So here's an example of using air condition ducting to transfer monkeys. Here's a large cage here. Here's a cage on wheels. What we could do is to lure an animal through the air condition ducting into this cage on wheels, and then if we wanted to take an animal down and introduce it to a new partner, we could just move the wheeled cage down, reconnecting the air condition ducting and have animals move into the cage without ever having to touch the animals. We collected urine samples very easily. Toni Ziegler, my colleague for the last 20-some years, I won't say exactly how long, has been very valuable in developing some incredible ways to get hormonal information out of urine samples. And we've realized early on that monkeys, very much like us, the first thing you do in the morning when you get up is probably go for the bathroom and pee, and one of the first things monkeys do when they wake up in the morning is to pee as well. 

And so what we had were we could get people to come in, wake up the monkeys early in the morning, walk around with a bucket under them, and collect a urine sample when it came out, and it gave us a way in which we could collect data from animals, monitor the reproductive state, monitor a variety of other things about them, which I'll show you in a minute, without ever having to capture and handle them. And, as I said, at the time this was a very unusual way to go. David Abbott and some of his colleagues from the Institute of Zoology in London have come up with some ways of using urinary assays, and we've adopted on that and expanded on those. So some of the hormones that we're able to measure, have measured in urine samples from cotton-top tamarins are estradiol and estrone, female hormones having to do with reproductive cycles; testosterone, which is involved oftentimes in aggression but also in parenting behavior; dihydrotestosterone, involved in sexual behavior; cortisol and corticosterone, which are stress-related hormones; prolactin and oxytocin, which are really interesting hormones that are involved in nursing and parenting and also in pair bonding; and luteinizing hormone, which is an important key for ovulation. And all these were things that when we first began the gold standard was to use blood samples. And the only way the endocrinologists would accept the work was if you had captured an animal, taken a blood sample, and measured the hormones from that. So it took a long time for various of us who were interested in developing noninvasive ways to argue and make is clear there's some clear advantages, both in terms of minimizing stress to animals, but also some clear advantages in terms of the quality of the hormonal data that you can get, especially looking at long-term hormonal effects that we can get by using urine instead of some other method. Toni Ziegler has gone on to expand this work to help other people around the world who were interested in looking at hormones. This is just a list of the species where Toni Ziegler has used her expertise to help develop noninvasive hormonal work. The species that are sort of bolded are endangered species. 

So you can see that she's doing a lot of work to apply these assays to help people understand the reproductive biology and the stress physiology of animals living in the wild, and it's a very important role for understanding wild animals. And here are some of the hormones that Toni's been able to help people measure in field studies: cortisol, testosterone, dihydrotestosterone, estradiol, and oxytocin. The myth number two was that parents are able to take care of their young by themselves. And let me focus on the green data first, the green bars. Show data we've gathered in the field, keeping track of those infant survival like in the field as a function of how many helpers were there in a family group. So one helper means that there's a mother and a father, the father is a helper. And with increasing helpers you can see that we found that there was steady rise in infant survival rate until we got to group sizes of five, a mother plus four helpers. And only then did we get 100% survival rate in our field studies. We then came back and I looked at our captive data asking the same question, and much to my surprise we found exactly the same thing happening in captivity. Even though animals were well fed, they had access to food, they didn't have to run away from predators, and what we find is that in our captive populations animals, infant survival reaches 100% only when we had family sizes of five or larger to be able to help take care of kids. 

So this creates some interesting questions about why are these helpers important? Why even in captivity are they so important? Secondly, it says we can't really house the animals in pair cages. If we want them to breed successfully, we have to have larger cages big enough to hold whole family groups together. And there's one other important question I'll get to in just a second. In is data from one of my colleagues, Sofia Zahed, which found that parents' effort is reduced by increasing number of helpers. So fathers show the greatest influence of having extra helpers around, they carry less and less. But mothers also show an effect where by the time we get to family sizes of five mothers are doing much less caring then they do before. Remember, mothers are the ones who have the greatest energetic load, they've just giving birth to two really heavy twins, they're nursing those twins, and they're pregnant again. And so reducing the load on mothers may have a really important role to play in infant survival too. And males carry more than females. This is looking at sub-adult and adult males and females, older brothers and sisters. 

And you can see that brothers do about twice as much infant care taking, especially as they get older, as sisters do. So infant care taking is a male affair, not so much a female affair. But parent skills are not innate, as people thought when they were working with these animals when we first started. These are data from a woman named -- who had done a lot of work with a another related species of marmoset. This is showing survival rate as a function of did a monkey grow up in an environment where she or he had a chance to care for somebody else's infants. So when both animals are experienced and both parents have grown up in a family where they could take care of somebody else's infants, we have 100% survival. If both animals in the pair are naive, that is they've grown up in a family where they have not had a chance to take care of infants, survival rate is below 20%. And we can see that mother's naive and father's naive give us intermediate values where one partner is sophisticated and experienced. What this show, I think, is that parental care experience is really important. But this is a different species than the cotton-top tamarin. 

So let's look at cotton-top tamarin data. This is not from our lab because we never raised any animals that did not have experience in their family groups. But if we look at here, we find two different experiences going on. First of all, let me call attention to the bar graphs for the inexperienced animals. They're in purple, I think. And you can't see them because in this particular study with cotton-top tamarins, there was not a single surviving infant to parents who were rearing infants without having had experience in their own family groups. So the only animals that were successful were animals that had grown up in a family group where they could care for somebody else's kids, and even when they did it the first time they weren't nearly as good and successful at caring for infants as they were when they bred subsequently. So we have two types of learning effects. Animals have to have experience in their family groups to learn how to care for infants successfully, and secondly, even first time parents have trouble keeping infants alive and they have to get some experience. So learning plays a really important role in parenting. 

And I oftentimes question freshman in my classes, why do we have to take drivers training classes and a drivers test and we don't require people to take a parent test and pass a parenting test in order to become parents? They usually get offended by that question, but I think it's something we need to think about for ourselves as well. Cozy cages are not going to be large enough for family groups. The US Department of Agriculture provides minimum standards for cage sizes. And I'm putting this in volume here because volume is what matters. These are arboreal animals, as I said earlier. They like heights. So the USDA minimum cage size volume is here. Our pair cages were this size, and this is the volume of our family cages that would house families with multiple kids. I was trying to translate this to human terms, and my wife, Ann, suggested I should think about this and translate it to floor space. So a monkey weighs about 100th of what an average human weighs. 

So if we think an average human weighing about 150 pounds and a monkey weighing a pound and a half, if we calculate the floor space, the USDA size minimum cages would give you about 270 square feet, about the size of a good sized dorm room. For a pair living alone without reproducing, they had 1900 square feet, which is a moderately sized, it's just a nice sized house to have. And the family groups with four to six kids would have close to the equivalent of 6,000 square feet to live in. But, as I said, volume is more important than mere floor space for these guys. So large cages seem to be really important for us, too. As I mentioned before, we had some arguments with veterinarians when we first began because we wanted to use wooden surfaces and ropes and things, as I'm showing here. Tamarins are clawed primates. They don't have fingernails, they have claws. And when they climb they have to get their claws into something. So if we had stainless steel surfaces or plastic surfaces, what are they going to get their claws into? So it felt very important for us and we managed to convince veterinarians, and ultimately now the USDA inspectors who come through are very happy to see a lot of soft surfaces, but soft surfaces like branches, ropes, and things like this are very valuable for keeping animals happy and giving them surfaces that they can climb on, they can jump from one surface to another. 

And yes we do still worry about sterilization, so we clear out these branches and ropes every three months or so, put in a whole new set of things so the animals have a chance to learn a whole new set of motor skills as they have new branches and things to do, to climb up. And finally, we've done a couple of studies to show that tamarins do not have any sort of innate fear of predators. We've put snakes in their cage, fed boa constrictors, and they showed mild arousal and curiosity to a boa constrictor but don't show any innate fear response. We tried to condition animals to become afraid of snakes because we thought if we're ever going to return animals to the wild, we need to make sure that they're not going to be caught by snakes, and there's a wonderful photograph in a book on another endangered species, the golden lion tamarin, that had a radio collared animal was that tracked and the trackers found the signal coming from the belly of a boa constrictor in Brazil. So, in fact, learning about snakes and learning about other predators is something really important for these animals. We also showed that captive born tamarins had no selected fear response to vocalizations from predators compared to non-predators. So what this has are important implications for reintroduction of animals and also suggests something very important. Overall, the theme I'm trying to get at is that learning skills, basic survival skills is something that's very important and a good captive environment should be one that gives animals the normal social background, the normal social environment so that they can acquire these skills that are important to survival. So we began with 11 monkeys in 1978 as a donation from a friend of mine in California who was doing research with them and was no longer interested. We, since 1978, have successfully bred enough animals so that we've given nearly 300 away to other places. 

To zoos, to other noninvasive research institutions, many undergraduate colleges are now training their students on how to work non invasively with tamarins, and some have gone to sanctuaries as well. Our oldest monkey lived until she was 27 years of age, older than many of the students who worked with her. So again, it's kind of remarkable because for an animal that's as small as one and a half pounds to live for as long as 27 years is a really remarkable life span for an animal with a high metabolic rate and small body size. So, just to summarize some points about the value of research, and I'll give you some research examples in just a couple minutes. We must learn to breed animals successfully and that requires some careful research on how to do that. Once tamarins are extinct we can't study them anymore, so I think we have a moral imperative to learn about them. If we can come up with some interesting research findings, I think we can also make tamarins more interesting to other people and maybe get others involved in conservation. And I want to make a really clear point here that I don't think nonhuman primates are little humans, little furry humans, I don't think they're good stand-ins for humans, so the reason for studying them and why they're interesting to humans is a more subtle reason than simply saying they're a good stand-ins for humans. And a good example for that is chimpanzees, which are our close relatives but they're highly aggressive toward one another. Males kill infants frequently. 

They mate promiscuously and we may dream of doing that but few of us actually get around to get that opportunity. And more interestingly, perhaps, for our own sanitation purposes, the chimpanzees think nothing about defecating in their beds at night. So is this the species we want to use as a model for understanding human behavior? For some reasons, some things, they might be very valuable for but there are some other ways in which chimpanzees aren't so useful. But the more subtle point is that variation across primate species can lead us to new ways of thinking about human behavior and new questions to ask and study about humans. And as an example, I want to just briefly touch on work my colleague Karen Strier has been doing for the last 30 years in Brazil with an endangered species, the muriqui monkey. And muriquis are really interesting because there's no obvious dominance hierarchy and no obvious aggression occurring between animals in the wild, and this raises some interesting questions. If we're concerned about our own aggressiveness and want to know something about how we might adapt our lives to being less aggressive, then having the knowledge that Karen is gaining from studying muriquis in the wild may have some potential value for us. That's a source of variation that we usually don't think about that can be a value to us. Tamarins are one of the few primates that live in families, and they can help us, perhaps, think in new ways about human families. So how do fathers and others become involved in parenting? Are the communication skills and social skills that result from family life make their cognition better? And are family species, living species in general, more helpful and cooperative than other species? So let me come back to the questions I raised at the very beginning, why are tamarins interesting? How do they maintain monogamy? What behavior is important and what hormones might be involved in maintaining a close relationship? I mentioned already that twins weigh a lot. 

Mothers have cost they incur from pregnancy and nursing. Fathers carry infants and we find even captivity with all the food they can possibly eat, fathers still lose up to 10% of their body weight within the first two months of when infants are born when there are no helpers. We males face a really interesting problem in that every woman in this room obviously knows whenever she's pregnant and knows that the babies she produces are her own, but none of us men can ever been 100% certain, unless we do a paternity test, that the babies we're helping to take care of are our own. So a good relationship with a good solid commitment to one another is something that's very important, especially for male primates. Grooming and contact are one of the ways in which this can be maintained, and we know that grooming with increase brain opioids, can reduce heart rate, reinforces learned behavior, can increase two hormones that are important in reward systems, prolactin and oxytocin, and grooming can also reduce cortisol. There's also some recent evidence that suggests being the one who does the grooming, not just being groomed but doing the grooming also provides a lot of benefits. So the individual who engages in the grooming behavior benefits physiologically as well. We found, interestingly, a series of asymmetries in grooming behavior. And this graph shows the percentage of dyads in which in tamarins where male groomed their mate more than the reverse. We find in wild marmosets as well, males grooming their mates, in 100% of the dyads males groom their partners much more than the reverse. 

We also find in wild marmosets that parents groomed their helpers significantly more often than the reverse. From a male's perspective, maybe I should be anxious about my partner. If I'm not sure about my paternity, then I should be the one to invest some effort into helping my partner be comfortable, be happy with me, and so this asymmetry we're seeing may be really important. Tamarin and marmoset monkeys spend up to 20% of their day in the wild grooming each other. So grooming plays a really important role, I think, in helping them stay together. Animals also engage in frequent nonconceptive sex. And what I mean by nonconception is we look at the female's ovulation date here, we can see that we can go back two weeks before ovulation or forward two weeks after ovulation and you can find that mating behavior, copulation behavior, is completely, I hope you can see this, completely unrelated to when ovulation occurs. This is curious because in most animals and most mammals, copulation is really tied to when females ovulate. And females oftentimes signal when they're ovulating to one another. We know that tamarins also do signal to each other when they're ovulating, so males are sensitive to odor cues that females give off that change when females are ovulating. 

But nonetheless, even though males can identify when females are ovulating, they're still mating with each other throughout the entire cycle. There's one other species that's very reminiscent of this, which is our own, where we mate with each other throughout the cycle and where we oftentimes have sex outside, at times when ovulation is not important. This raises an interesting question, why is there so much sex and what value might it have? Why is it not linked to ovulation? Suggested to me that there might be some social functions of nonconceptive sex just as there's social functions to grooming. And to examine that we started looking at some hormones, and two hormones that seemed be of interest were prolactin and oxytocin, which we know are important in infant in lots of female mammals. And we know from research done by several people now that oxytocin is involved in pair bonding, especially in female rodents that are monogamous. We also know that in humans at orgasm we find increases in oxytocin and prolactin in both men and women at orgasm  suggesting that these hormones might have something to do with the reward of engaging in sexual behavior. So we asked the question of our tamarins, does variation and affiliation with their mate have any affect on these two hormones, oxytocin or prolactin? And can we identify different variables that might explain variation in these hormones that might suggest different roles for females and males in terms of what it takes to maintain a good relationship? So this is a figure that simply shows that this is looking at female prolactin levels related to how much affiliation behavior they engage in with their partner. And you can see there's a very clear and positive relationship. The more affiliation someone has, the higher her prolactin levels. This works for males and it works for the pairs as well. 

If we look at the hormone oxytocin, we also find a similar relationship that is as affiliative behavior increases within a pair, their joint oxytocin levels show an increase as well. And even though oxytocin has been looked at primarily as a female hormone, looked at in pair bonding in females, we found in tamarins that male and female levels here, male levels here, were very closely related to each other so that if we knew what the level was in a male, we could predict the level in a female. So overall we found within the species a 10-fold variation in the amount of affiliation, a 10-fold variation in how much oxytocin levels they demonstrated, but no difference between the overall levels of males and females. However, we did find that what explained the variation oxytocin differed for the two sexes, maybe in way that some of you would find very predictable which was that variation in male oxytocin was explained by how much sex they had. Variation in female oxytocin was explained by how much cuddling and grooming they experienced. I got really excited about this result when I found it and went home and mentioned it to Ann and she just said, well, duh. [LAUGHTER] But I think it's interesting because we're told what's appropriate behavior for us to engage in. We have a culture, we have religious rules that tell us what to do. Here we have some animals that are not subjected to the cultural norms that we have and not subjected to religious rules that tell them how they should behave with one another. What we're finding is that for them the same sorts of variables seem to be important as we think are important for humans as well. 

And one final point to make about these animals that I found really remarkable is that females, in the pairs that had the highest levels of oxytocin, frequently solicited sex from their partners. And males in those same partners also initiated cuddling and grooming with their partner. So the best pairs, the ones with the highest levels of oxytocin, were the ones where each partner met the needs of their mate. And I think that's something important for us to think about for ourselves, too. So next part I want to talk about briefly is how do males, fathers and brothers, become good infant caretakers, what's the role of learning, and looking at hormonal changes. So I've had to label this figure now male carrying infant because typically when I showed this picture people would say, oh, look at the mother and her baby. And it's almost never the case that you'll see a mother carrying a baby on her back like this. Mothers will carry babies primarily to nurse them, but they rarely carry them on their back. As I've shown you already, it's up to fathers and brothers to do most of the infant carrying. We find that fathers have prolactin levels that are just as high as nursing mothers. 

So this hormone prolactin, which we used to think about as primarily involved in nursing and producing milk for females, is something that fathers show at the same level as mothers do, but curiously prolactin levels in fathers increase prior to the birth of infants. And we find a lot of other hormonal changes occurring in experienced fathers halfway through their pregnancy. One other thing that turns out to be very important is that mothers must allow fathers and others to access their infants, and I think this also has some relevance for humans as well. This is a complex figure but let me call attention to two major things. One is that the upper graph in every case shows hormone levels for experienced dads and the lower graph, those triangles, shows first time fathers. And you can see that there's some very clear differences between experienced fathers and first time fathers and hormones. Testosterone, not much difference in dihydrotestosterone. But look, here's estradiol and estrone, two female typical hormones which we're seeing develop in males, especially experienced males, over the course of their mate's pregnancy. And we find prolactin levels are changing in experienced fathers fairly early in the pregnancy, but in the last month, first time fathers' prolactin levels also increase as well. So what we have is some remarkable changes in the hormonal milieu of male caretakers during the course of their mate's pregnancy which begs the question how do they know that their mates are pregnant. 

You come home, a human woman comes home and says, hey honey, guess what? The doctor confirmed that I'm pregnant. And we all rejoice and take pleasure in that, usually. But how does a monkey communicate to her mate that she's pregnant? How does he know halfway through pregnancy to start changing his hormones? The one possibility that we've found is that fathers' hormones start changing, we find a type of hormone called glucocorticoids that starts increasing within a week of when we think the fetal adrenal gland begins to create glucocorticoids, and the mother, stuck with these extra glucocorticoids in her body, excretes them to the outside. So we find that the mother, halfway through her pregnancy, begins excreting very high levels of these stress-like hormones glucocorticoids and within a week of when she starts excreting those hormones, fathers, experienced fathers but not first time dads, start showing changes in their hormones as well. This raises the tantalizing possibility that the fetus is excreting something using the mother as the vehicle to change the behavior of the father and get the father's hormones ready to be prepare. This raises all sorts of questions about, this raises all sorts of questions about human fathers. People have not really looked very closely until very recently at what hormonal changes might occur in human fathers and when in pregnancy do these changes occur. And what this suggests is that there may be some interesting, important hormonal changes that occur in human fathers during their mate's pregnancy and there's also some potential signal mechanisms that we're learning about that are important for what might be cues for males to pay attention to in their pregnant partners. Experienced mothers have to let go, find that they do let others take care of infants but one of the problems with first time mothers is they hold on to their infants. These are data from the wild in Colombia. 

And what we see is that about 90% of the time for week one and week two, first time mothers monopolized control of the baby and rarely let someone else take care of it. By contrast, experienced mothers who had had multiple pregnancies, spend about 50% of  the time in the first week taking care of kids, but by the second week they're down to the 20% that they're going to spend the rest of the time. So one of the things that becomes really important is if you're going to have other animals or other individuals in your family take care of infants, it's important for mothers to let go of the infant care and let someone else take over. And experienced mothers in tamarin families in the wild seem to know how to do this. First time mothers don't seem to have that skill. How do parents keep others from breeding? There's been a lot of work done on reproductive suppression in tamarins and I just want to touch on this very briefly. This is a study we did looking at 31 animals over the course of a couple years each because we weren't convinced that animals were totally reproductively suppressed. But every single daughter that we looked at never ever did we see any signs of ovulation while animals were living at home. And we wanted to see what the cues were for this so one study we did was to transfer mother's odors to daughter's cages after daughters have been moved to giving a new mate. And we found in every single case that we transferred mother's odors on a daily basis, none of those females ovulated while their mother's odors were being presented. 

So we find that mother's odors play an important role. But something else is also important. We can take females away from their mother but house them with a familiar male, their father or their brother, and we still don't get any ovulation occurring. And only when animals are either paired with a novel male or housed adjacent to a novel male do we find ovulation being released and occurring. So novel males play a really important role in terms of reproductive suppression as well as to signals and cues from the mother. Both of those are important and I think human families, I suspect a lot of mother/daughter conflict in human families might be alleviated if mothers could be more assured that their daughters were reproductively suppressed while they were going through their teen years. [LAUGHTER] And here we have animals that have very stable family relationships, and it's a nice way to keep others from competing with the mother for the breeding position. And finally, the last part of what I want to talk about is, does cooperative breeding lead to better social learning and cooperation with others? There's been a lot of studies in recent years but I'm going to just give you two examples of how tamarins, in this case, how tamarins rapidly learn about a novel task from watching others. And Liza Moscovice developed a special frame that we could hang inside a cage. There are five different targets here that can hide food. 

In this case, the food is behind the green door which is propped open and you can see a piece of food here. Each of these other containers has food behind it so that the odor is controlled. And what the animal has to do is to locate the unlocked container, and it has to learn a new motor task because animals have never before had to perch here and use their hand to move a door from one side to the other and reach in with the other hand to get the food. So learning a novel motor task, you also have to learn where the food is located. So we gave individual animals within a pair a chance to learn this task. And then after the task was well-learned, we tested them with their partner, and the really important information here is how quickly does the partner learn when its mate already knows how to solve the task. And what we found was that social learners, the partners were really interested in the apparatus, they followed very closely on the demonstrator and very quickly learned the correct site. When they got there, they also learned how to master this novel task of moving the door open. But when these animals came, this animal had already taken the food. So we have animals that have learned a new task, a novel motor skill, without ever getting reinforced for doing it but they're doing it in part because their partner has just done it in front of them. 

And if we look at how quickly they learn to get to a novel forage site, within eight trials all eight animals that were tested socially acquired the test within just eight session, eight chances to learn this. Individual learners took a lot longer. Only two of them learned a task within eight trials. And animals who were just allowed to interact socially with each other without anyone knowing what to do, not a single one of them solved this task within eight days of testing. So social learning occurred much faster than I've seen occur in any other chimpanzee study, and it occurred without any rewards. And when we tested these animals a year and a half later, they were still able to solve the problem right away. So they had a long-term memory for how to solve the task. So some other examples that we've done, we find more rapid reversal learning than any other species to date. We find that animals teach their young about what food to eat and how to eat. We find that adults will help their juvenile kids learn how to solve tasks. 

When they're presented with a novel and difficult task, parents will spend time helping them, but they don't help each other when they are adults. And we found no evidence of teaching in chimpanzees that's anywhere comparable to the types of scaffolding behavior and teaching that we find in tamarins. So again we find a clear difference between what tamarins are able to do and what chimpanzees do. This has led some anthropologists to start speculating on the idea that maybe cooperative breeding is an important type of social system that fosters teaching and social learning. And one theory has recently argued that we've learned, we as humans have acquired a lot of technical ability to learn about tasks from other animals like chimpanzees that have large brains and can learn individual tasks really quickly, but what makes us uniquely human is the ability to combine the learning types that chimpanzees do readily with the type of social learning and teaching behavior that tamarins show and that, therefore, the combination of these two sets of skills, the big brain of chimpanzees and the social environment of family living, might contribute to the complex cognition that we humans show. Tamarins naturally cooperate with each other. Here's a apparatus where there are two pieces of raisins and both animals have to pull these trays simultaneously from either end in order for anyone to get the food. And we find that they learn that spontaneously very, very quickly. We can also manipulate the apparatus. This is showing a diagram, and there are two holes that can be lined up. 

We can either have two pieces of food, one on either side, or we can have a piece of food so that only one animal gets rewarded but both animals still have to pull for the reward to be obtained. We can have a single reward in the middle or we can place the reward over here by one animal but we have this trough that lets the food reward roll down and go to the animal on the other side of the cage. One of the interesting questions is, how well do animals solve these things as a function of whether they're always getting reward or not? So here we see where both animals are getting rewarded the solution rate is about 98% of the time. Even when there's reciprocity, when I get the food today and I get all the pieces of food but you get it tomorrow, there's still a very high level of cooperation. Both animals still continue pull at a very high rate. When the food is available and we both have to scramble to get it, still is pulled at a high rate. And even when the reward is being delivered to the animal on the opposite side of the apparatus, the animals still continue to perform about 50% of the time. And I want to contrast this with work on capuchin monkeys which are oftentimes talked about as a model smart monkey. And you can see that when someone else did the same parallel types of tests with capuchin monkeys, they solved the mutual task much less often and when reciprocity was involved, they showed only half as many correct solutions as tamarins do. So again we have mutualism and reciprocal reward with success rates much higher for tamarins than for capuchins and chimpanzees tested in similar ways. 

So to summarize and finish up, cotton-top tamarins are highly endangered species, very vulnerable to extinction in the wild. We've been able to create a successful captive breeding program starting with 11 monkeys 30 years ago, and we've donated close to 300 monkeys to other places as a result of our success in captive breeding. We think part of our success is due to housing monkeys as families in large naturalistic cages and keeping offspring at home long enough to be able to learn parenting skills before they go off and try to parent on their own. And as I've tried to indicate, lots of other skills have to be learned as well. When we started using noninvasive methods we met with a great deal of skepticism because the traditional way of doing research was to use more invasive ways. Thanks to Toni Ziegler, we've within able to pioneer new noninvasive methods for studying hormones and expand them to a whole variety of species, and I think these methods are now the gold standard for field research with nonhuman primates and lots of other animals as well. So we have a very successful selling or extension of the work that began with tamarins to affect lots of wild populations as well. Other noninvasive methods that we developed have minimized handling of animals and allowed us to test animals in their home cages. A very important point is that we treated tamarins as our research partners. They're not subjects, they're our partners in research, and I think it's a very important mind set to have when you're working with nonhuman primates is to think of them as your research partners. 

Without their cooperation and collaboration we're not going to get very good research data, nor are we going to be as successful as we'd like to be in terms of maintaining them and breeding them into the future. Noninvasive hormone sampling allowed us to monitor reproduction but also allowed us to ask about hormonal changes leading fathers to parenting and why daughters do not ovulate. Results suggest new ways for thinking about increasing involvement by human fathers and care taking and has led very recently to new studies looking at hormone changes in fathers across pregnancy. Also helps us stress the role of experience. We require drivers training but not parent training, as I said earlier. And mothers have to learn to let go of infants and let others take care of them. Finally, tamarins show rapid social learning, teaching behavior, and cooperation that's not seen in most other nonhuman primates, but it's really similar to skills we see in humans. So does cooperative breeding foster these skills, and, in addition to the cognitive skills of apes, is this what leads us to make humans unique. Tamarins are not little human beings but humane, noninvasive research can not only help preserve the tamarins on into the future but help us gain insights into human behavior. Before I close, I want to acknowledge that I've been supported and blessed with a large team of really wonderful collaborators over the years. 

And this is just a few of them, people who've been involved in the work that I talked about tonight, but I've been really delighted to have such a large group of people who are all committed to the well-being and safe care and careful care of these animals where always the first priority was to maintain the animal's health and well-being as our first priority. I also want to acknowledge my wife, Ann Lindsey, who is a good critic, a very good critic, and helped me change a lot of things. And also, for those of you interested in learning more about cotton-top conservation, I want to refer you to a really important website that Anne Savage has developed, ProyectoTiti.com. It's a good way to learn a lot about the status of tamarins in the wild and learn a lot more about their behavior, and also, if you would like to donate for cotton-top tamarin conservation, it's a very good place to go and be able to make donations. And I'll stop here and see if anyone has any questions. Thank you very much. [APPLAUSE]