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]