Adaptive Specializations in Birds?

Psych 1090

Lecture 6

First of all, why did I choose these particular experiments for

examples in class?

Because they are particularly intriguing with respect to tying

together

brains, general behavior, nurture/nature and cognition

And, although many researchers find all the data

compelling,

others are not convinced and are arguing against the

conclusions

thus making for a good topic for discussion

And that will be a theme for several classes

Other systems in other species and lineages are certainly of interest as well…but we can’t

do everything

and birds are my strong point….

Several avian species appear to depend on food-storing for

survival

What we will be examining is whether this ability reflects a modularity that is genetically

determinedAnd how one goes about

determining the answer to such a question

What is absolutely clear is that

in the wild, some species cache and others do not

the extent to which various species rely on caches to survive differs

the time between caching and recovery differs across species

What is also clear is that

for some species, such as nutcrackers, we have very

accurate data concerning their abilities in nature

and for others, like chickadees, we do not

So that, in some cases, the choice of subjects to study

have more to do with their availability and ease of maintenance in the lab

than our knowledge that they would make good subjects for

study

We also do not know, for all the species studied

how their caching ability develops over time

In a paper by Clayton (Behavioral Neuroscience, 2001,115, 614-625

), we find that at least one species needs to learn about

storing for the ability to develop properly

In fact, birds prevented from caching

Did not develop a large hippocampus if they were

juveniles

Did not maintain a large hippocampus if they were adults

Such data suggest, as Elizabeth Bates once said,

that “modules are made, not born”

In other words, an organism may be born or hatched or spawned

with a possible blueprint for development

but experience is needed for the brain area involved to develop

All this is not to denigrate any of the studies we’ve read…..

but rather to remind you that even as well-designed as they may be…

other issues may be involved for which the experimenters did not

—or could not—control

And we really need to keep those ideas in mind as we

read these papers

Because these ideas may—tho’ I can’t at all guarantee—be the

reasons for some of the disparate results that we find

So, with all that in mind, let’s review what is known about avian

caching… caching birds seem to rely on some form of memory to retrieve caches

caching birds in general have larger hippocampal areas than birds that do not cache

the hippocampus in mammals is related to spatial memory

The question that Shettleworth raises, however,

is whether spatial memory is a particular adaptation, or whether

caching birds are just good at remembering things…period

And, following Shettleworth, we’ll discuss in some detail what is

meant by ‘specialization’…

morphological: specific physical traits such as long beaks

physiological: specific brain variations behavioral: caching itself

cognitive: specifically good memories

We can argue that a trait has arisen because of specific

selection pressures

but, correlation is not causation

Thus we have to test that the trait evolved because it really does

improve fitness

and isn’t just a coincidence

We can test this idea in several ways…

We can propose a model that can be tested against data from

nature:

If the data are consistent with the model

we can argue that it may accurately represent reality

What Shettleworth does not discuss openly

but that does run through her and her colleagues work

is the importance of having multiple competing hypotheses

and models

Because showing that your data are consistent with one particular

hypothesis

Does NOT prove that particular hypothesis

but only makes it one of several possible explanations….

Alternatively,

If your data are not consistent with a given hypothesis

you can rule out that particular hypothesis or model

And that allows you to look at one of a number of other competing

hypotheses or models

Performing experiments helps you obtain data to test various

hypotheses…

But you have to make sure that you’ve set up the appropriate

controls so that you are indeed testing what you plan to test

with internal and external validity

Remember that you NEVER should set out to PROVE your

hypothesis

but rather to test it to see if it holds up

And to ensure that you are open-minded about the results

The third way to test hypotheses is to collect

observational data

And sometimes that has to go first, so that you have enough of

an idea as to what may be happening

so as to be able to form a model

Shettleworth also argues for using nonhumans

because they allow us to see how adaptations have arisen

in conjunction with exploitation of particular ecological niches

In ways that are much more difficult to study in humans…

but not impossible…

Relevant to these lectures are the now famous neuro studies of

London cabbies …(Hippocampus, 13:250-9, 2003)

who must pass map tests to get their licenses

Compared to the average human

hippocampal areas in London cabbies were statistically

significantly larger than normal

and the size difference was correlated with the amount of

time they had been driving cabs

The specific questions that arise for the caching birds,

however

is the extent to which we can provide a laboratory situation

that appropriately tests what is going on in nature

One of the big issues in these papers is, indeed,

whether the so-called “contextual variables” of the laboratory

are responsible for the data

and whether there really aren’t species differences

As does Shettleworth, let’s start by looking at what we might expect to find when doing

comparative laboratory work across species….

good

poor

RI or memory load

A

B

When the retention interval is short or there are few things to remember, both are equal

As RI increase or lots more to remember, one species falls apart faster than the other

Three critical points:

No ceiling effect: there’s something that is making the

situation at least equally difficult for both birds at the beginning

The change in conditions affects one species more than the other

Both can do an easy task

good

poor

RI or memory load

A

B

No matter what happens, one is better

Might be due to general abilities…if a number of birds, not individual differences

good

poor

RI or memory load

A

B

Even when the retention interval is short or there are few things to remember, one is

betterAs RI increase or lots more to remember, one species falls apart even faster than the other

Such data suggest that even under easy conditions

One species is better than the other

And retains its advantage, even tho’ it is challenged as

conditions get tougher

good

poor

RI or memory load

A

B

When the retention interval is short or there are few things to remember, one is better

As RI increase or lots more to remember, one species completely falls apart; the other is ok

A kind of turtle and hare situation….

Which might seem surprising, but could come about in a

species that doesn’t have to remember much,

but has to remember it for a long time

Shettleworth also discusses the difficulty inherent in comparing tasks across

species

How do you know whether the different tasks really tap into

different abilities?

Sometimes that is truly difficult to determine

And, in a bird, with a brain that is very strongly weight and

metabolically limited because of flight limitations

[Heavy brains and overly full stomachs make flight difficult]

Various compromises need to be made

One issue that is not discussed, particularly for chickadees

is that their brains change quite a bit from fall to spring

areas for storing grow in the fall and shrink in the spring

For other birds, the same thing happens in reverse for song

centers….

Interestingly, chickadees have pretty simple songs and lots of

calls used year-round

Possibly leaving more space for storing?

But this brings up a matter introduced only briefly….

Keeping birds on a sorta fall light cycle…

Is that the only thing that mediates the changes?

I don’t think we know….

What if birds’ bodies cycled through without the light

cycles?

Unlikely, but I’m not sure it has been tested…

Or whether group living might have an effect wrt competition?

We’ll see next time that birds pilfer from each other….

Maybe operant situations, which don’t reflect such

pilfering, unnaturally affect some

results???

What about the relationship between hippocampus and any

avian memory?

I’m not arguing that such effects must exist…

Only that some of these are controls that haven’t been

done….

And might affect data…

Another issue is in what is involved in birds’ abilities to

remember where food might be obtained?

That is, how do foraging strategies affect the results….

maybe color is what attracts some birds to a food source, not memory

for place?

In these papers, Shettleworth compares caching chickadees

with non-caching juncos…

The former have relatively larger hippocampus areas than

the latter

Both seem to work fairly well in laboratory settings

The technique is operant spatially delayed nonmatching

to sample…

So birds saw two disks, side by side, with only one lit

They pecked the lit one and the lights went out

They then had to fly to the back of the cage

Then, WHATEVER key they had pecked previously would be

wrong

To get a reward, they had to switch

Chickadees overall had a better memory, whatever the

retention level….

If the birds could, just by chance, choose the SAME

sample they had chosen before

That is, if they could pick something and sit on it…

Then the juncos looked more like the chickadees, tho’ still a

bit less good….

Shettleworth argues that the issue is “interference”…

That chickadees are less likely to be confused by what happened in

a previous trial

That a bird that stores lots of stuff in different places better

be able to separate out different memories for different

eventsAnd both had trouble

remembering when their hippocampi were lesioned….

With chickadees fairing worse…

But how well does this task reflect the birds’ lives in

nature?

Would this possibly have to do with how well birds learn

where to find food?

For juncos, how often do they need to shift?

This idea comes up in the next experiment

where birds simply had to learn that it was win-shift, period

No samples to match or nonmatch,

Just keep alternating right/left

So why would juncos do so much better this time?

Even in initial acquisition?

Maybe the issue was external validity….

A bird that stores and retrieves, like the chickadee, is good at a

two-step process

But is less good at abstracting a one-step pattern?

Other studies compared caching marsh and non-caching blue tits (also parids; look a lot

like our chickadees)

The first task was a “simple” memory task, of finding food

designated by a mark

So bird saw something like this

Blue marks the spot where they ate a bit

Birds were then removed from the room for a bit of

time

Then allowed to return

Now the holes were covered

Not clear if sticker was removed….

Birds of either species had no problem

Researchers saw no difference in ability

But what if the holes were covered initially?

So now the birds were having to visit possibly several boxes

before finding the nut….

Once they got the nut, they were again excluded and then could

return

marsh tits had less trouble; could blue tits just not remember the

site?

Or was it an issue of interference of memory for

going into all the empty boxes?

Here the boxes were not clearly marked for the birds;

Position factors were the key

When Shettleworth next did what was supposed to be a replication with an operant

procedure

The results were unexpected….

Let’s look at what the birds had to experience…

At first, each of these were rewarded….

Then birds saw

Followed by

or

or

Juncos did better than chickadees at choosing the

most recently observed sample

The technical explanation is that the juncos simply did

recent association

and chickadees had recognition memory…

But in terms of ecology….

Chickadees store a bunch of stuff in different places

And don’t necessarily retrieve them in order

But have to remember them all

But these tasks don’t necessarily emphasize the difference between spatial skills and other forms of

memory…

What would happen if you pit various forms of spatial

information against something like color or pattern?

So, you give birds that kind of choice…. “x” marks food

x

Then the bird experiences this:

And the chickadees choose in a standard pattern with

respect to spatial cues first and color last

Juncos went to a feeder that did match the sample at some

level, but randomly with respect to color versus

location

An issue mentioned only briefly involves seasonal effects….

Chickadees store for very short periods of time in nature…at most

only a few hours

in the summer, colors and patterns won’t change

In the winter, a quick storm might cause differences over a

brief time period

And, of course, brain areas for storing grow in chickadees in

the fall…

Maybe in summer their brains are closer to those of juncos?

Other issues, only briefly mentioned, involved the visual fields used for close-up versus

distancewhich likely have some effect on

how the bird is locating a box in an aviary

compared to hitting a button on a screen….

tho’ that may have been controlled

And possibly the differences between juncos and chickadees

Which is different from how well they remember these types of

information…

have to do with how quickly and well they encode various

forms of information….

One might come up with any number of ‘just-so-stories’ based

on the need to grab several seeds at once

and find hiding places without being seen

and somehow coding these sites

As opposed to just remembering in a general sense where food might be

And sorting through food versus non-food types of things

while competing w/ several other birds in your group…

In general, Shettleworth argues for a modular approach

which is fine as long as we are open to the possibility

that these modules develop and are maintained by experience

And, we have to recognize that a module is considered

a processing center…

Not necessarily a memory storage site

Although some researchers interpret modules that way

Now, in the next paper Shettleworth performs

experiments to tease apart

the issues of color versus location in caching and

noncaching birds

One important point is the argument that color vision in all

passerines is similar

But that of course doesn’t mean that the birds’ spectral

sensitivities

are necessarily tightly connected behaviorally…

All humans have pretty much the same color vision

but different groups have different ways of color labeling

So we need to keep that in mind when comparing the work on

juncos and chickadees…

particularly when using color discriminations that may be valid

for humans

but might be different for birds

So, even on the experiments that pit location against color

and the chickadees choose with respect to location and the juncos

randomly

Lots of reasons may be—tho not necessarily are—involved in their

choices

Which is why Shettleworth tried to tease apart species differences in

attention to color vs shape

spatial versus color memory

spatial discrimination

Interestingly, most studies to examine how subjects respond

to compound stimuli use things like

vs

or

But such tests really seem quite confusing as nothing in the choices really match the

original item

which is why Shettleworth’s compound

makes a bit more sense

So, the birds saw a variety of possibilities….

or

Or a similar task but with only a color or shape as the

initial sample

The only reason I can fathom as to why the birds never saw

something like

Pitting color versus location

was that Shettleworth wanted to emphasize

that the compound stimulus could indeed be dissembled

into its component parts

and those parts tested independently

Interestingly, both species had lots of problems overall…

At least over a thousand trials before reaching statistical

significance

And both species really had trouble with a color choice after seeing the compound sample

But, overall, the chickadees eventually did better than the juncos on the location trials

And the juncos did better than the chickadees on just the color

trials alone

suggesting that location versus color differences did hold up

somewhat

The next experiment didn’t deal with the compound stimuli

But gave the same birds the location only and color only

tests

to see what would happen when the birds had to remember the task for longer times….but less

than 1 min

Supposedly, in the wild, chickadees cache for longer

periods than that…And note that Shettleworth is

careful to argue that the chickadees maintained their

hippocampal size

because Clayton argued that experience was necessary to

maintain a large hippocampus

Interestingly, chickadees forgot locations faster than the juncos…

which doesn’t jive with what one might expect in the wild…

But in the wild the birds are actually storing something

Then remembering the site

Here the birds are being asked to remember something not

associated with food in order to get food….

So maybe the task was more unnatural for the chickadee than

the junco?

In the third experiment, Shettleworth wanted to find out if cachers and noncachers differed

indiscriminating locations that were

‘close’ versus those that were ‘far’

‘close’ and ‘far’ being somewhat constrained for a touch screen

So they compared results for trials like

vs

They found no species differences for difficult, ‘near’

trials

but chickadees were a bit better on the easier, ‘far’ trials

And both birds more or less coded space similarly

at least for this kind of task

My personal “take” on this work is that species differences do exist

And that often the operant-type experiment does not reflect reality well enough for these

differences to show up

And although the lesion data are compelling in terms of

impaired performance

What might be impaired is the ability to form memories and

process information

rather than the ability to recall information

But let’s look at other operant studies on species

for which much more is known about their natural

behaviornutcrackers and various

types of jays

Here, all species cache, but to varying degrees

And many experiments have shown that those species that

are most dependent upon caching for survival

nutcrackers and the pinyon jays

perform better on tasks of spatial memory

than scrub and Mexican jays that do not

But, as we wondered for the chickadees….

Were some jays just smarter overall or were they specialized

for spatial memory?

So they had to be tested for nonspatial memory tasks

Now, some minor issues that might be of importance as we

look at the Kamil-Balda work….

First, birds were on a summer-like light schedule

Such was set to encourage caching as they would in the wild

But what about retrieval?

Also, the amount of caching each bird was doing varied…

That caching is necessary to maintain large hippocampus area

and the ability to cache

and birds’ histories might be important

was not known at the time this work was done

Another issue, not known at the time,

was that birds that prefer to cache degradable items

might perform a bit differently than seed-cachers

We’ll talk more about that next week

For now, let’s just look at the studies….

The nonmatch color task was similar to all the others…

The bird saw

Followed by

And birds were trained til they hit the nonmatch at

85%

What they then did was to test how long the birds could

maintain their memory for the sample

When the bird was correct, the next trial had a longer interval

When the bird erred, the next trial had a shorter interval

They analyzed the data with respect to speed of

acquisition as well as how long the birds could

remember

Scrub jays were overall slower than the pinyon and Mexican jays

The one slow nutcracker may have made that species look

‘bad’

The really interesting result here was that pinyon jays and

Mexican jays did somewhat better than the nutcrackers and

scrub jaysThus overall memory (not spatial in particular) had less to do with

caching

than with their sociality…

Possibly the birds that lived in groups—the pinyon and

Mexican jays

had to rely on some kind of pattern memory to recognize

several individuals

whereas the other jays did not

But Kamil and Balda had to make sure that there wasn’t anything strange about this

group of birds

So they gave the same birds a simple nonmatch-to-sample

spatial test…

Birds thus saw

Followed by

And they had to choose the opposite location

from what they had seen

After reaching 85 % criterion, they experienced the same

titration task

and researchers found this time that the nutcrackers were

special

They learned faster and retained the information

longer

What was surprising was that the pinyon jays didn’t do much

better than the scrub or Mexican jays….

They had done better in other spatial memory tasks in previous experiments

Again, one wonders about an operant task..

Interestingly, tho’, the pinyon jays’ hippocampus is more like that of the scrub and Mexican

jayswhereas the nutcrackers’ is much

larger

Which makes one wonder why the pinyon jays did so well on the

other tasks…(e.g., radial maze)

Other data on woodpeckers who cache (Volman et al., Brain Behav Evol, 1997,

49:110-120)showed that those that cache the most may have smaller

hippocampal areas than those that don’t store at all

Leaving the correlation still open to discussion

Specifically, what else in the birds’ lives may be impacting the relative sizes of their brain

areas?

Possibly the large home ranges of the noncaching downy and hairy

woodpeckers require lots of spatial memory for finding food

sources?

Or maybe these species do cache but do so in a manner

not discovered by researchers?

Or maybe the noncaching species have more holes that they use for shelter in their large territories that need to

be remembered?

The issue is that food storing is but one metric that can be used

to examine spatial memory

And thus researchers should not be caught in a tunnel-vision

with respect to that trait

So let’s look at a task that is more similar to the birds’

natural situation…

This time they let birds cache seeds in a room with lots of

holes in the floor

each hole was actually a sand-filled dixie cup

Chamber looked something like this…

pegs and holes alternating, w; rock

landmarks

Birds were allowed to cache up to 24 seeds per session, but

usually cached fewer

and were given up to 6 caching sessions to get 12-24 caches

They weren’t allowed to use a given site more than once, and

only 62 sites were available– about ¼ of possible holes in room

They then had four recovery sessions…

Using a fourth of what the birds had cached…i.e., about

6 caches

With all other cache sites plugged

I had to go to an earlier paper to figure out the

clusters….Each good cluster had 6

contiguous holes with one seed/cluster

Bad clusters had no seeds

So birds had about 5 or 6 good and bad clusters available

So again about a quarter of the room’s holes were

available….

Except that most of the previous cache sites were now plugged

And only sites not used plus a subset of used sites were

available

In general, there was no difference in how many caches the successfully caching birds

madeSo that comparisons could be

made across species

In general, Mexican and scrub jays made about the same

number of errors at every time interval

Whether the interval was 10 days or 250 days

They were just slightly better than chance

And the individual differences were scattered all over…some birds even improving a bit w/

time

The nutcrackers and pinyon jays were particularly good at shorter intervals…10-60 days

Interestingly, they didn’t do too much better than the other birds

at the longest interval

And individual data are a bit strange…

These data contrast with other studies that showed that

nutcracker were particularly good at very long intervals…

And here nutcrackers couldn’t discriminate between good and

bad clusters

One possibility is that in reality the nutcrackers would

be recovering caches on a daily basis in the wild

Which they would have to do to survive

And that such daily recover keeps their hippocampal areas large

Whereas in these studies

they didn’t do anything for months at a time

Which may have been a real difference from the other

studies as well

Remember, when this paper was written, no one knew

that experience was necessary

in order to maintain hippocampal areas

Given what happens in the wild, these data just don’t

make major sense

So, again, we are left with issues of internal and external

validity

The need to know lots about the animals’ prior history

about their ecology, their social structure, their brains, and

more…

One big issue—from a seminar last year—is the connection

between the hippocampus and other parts of the brain

In humans, at least, many connections exist to the parietal

cortex

an area that seems to involve attention

And, of course, attention is the first step in any of the tasks

we’ve discussed

So what might be important is not just relative hippocampal size

but the type and number of connections to the avian equivalent

of the parietal cortex

or the relative size of this area

And, because parietal cortex is involved in all attentional issues

from number concepts to communication to spatial issues

a balance between parietal and hippocampal areas might explain

contrary data

We know, for example, that areas relating to general cerebral

cortexvary considerably across species

Certain areas relating to things like insight detour are relatively small in pigeons and relatively large in

crows and parrots

and success varies with size

So, if birds see

Pigeons and chicks, not crows or parrots, take a long time to figure out how to go around

And in monkeys, lesions to one part of the cortex messed up

the ability while lesions to other parts did not

Although this is a different spatial task than caching,

you can see the relationship

And possibly how it is not just size of one area but the

interrelationships

that can indeed be the critical issue

Overall, these studies provide fascinating insights as to what these creatures are

capable of doing