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>> 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]