(CROAKING)
Amphibians were the first backboned animals to leave the water
and colonise the land.
Today there are some 6000 species of them
and new ones are constantly being discovered.
We may not often see them
but during the breeding season we certainly hear them.
(CROAKING)
Choruses like this ensure that we are well aware of frogs and toads.
But there are others kinds of amphibians that dont make themselves so obvious.
Newts and their close relatives the salamanders.
And even ones that have completely lost their legs.
But all amphibians have one thing in common
a moist skin.
If that dries they die.
And dealing with that danger dominates their lives.
How are they to survive away from water?
Four hundred million years ago
the only backboned animals on the Earth were fish.
The land was empty except for insects and other invertebrates.
But then one of those fish managed to haul itself out of the water
and up on to the land.
You can see what sort of creature that might have been
if you go to north-east Australia.
There the rivers only too often dry up.
But one remarkable ancient and extraordinary fish
manages to survive
because it has a rare talent for a fish.
It has lungs and can breathe air.
And theres one at my feet right here.
Fossils just like it date from precisely the time
when the great invasion of the land took place.
On occasion it rises to the surface and gulps air.
The air goes into a pouch that opens from its throat
where the oxygen from it is absorbed.
This is a lungfish.
It punts itself along the river bottom using two pairs of fleshy muscular fins
placed low on its body just like simple legs.
Sometime around 360 million years ago one of its remote ancestors
used such limb-like fins to push itself up onto the land.
That pioneer may have looked much like this strange monster
that haunts the waterways of Japan.
Its the giant salamander the biggest of all living amphibians
that grows to a metre or more in length.
It too has lungs and breathes air
but even so it almost never leaves the water.
Males make their dens in both natural and man-made retreats in the river banks
and defend them against all other males.
A newcomer arrives looking for a breeding den of his own.
It wont be here.
The resident male has good reason to be so defensive.
He is guarding a batch of eggs left by a female
who visited him a few days earlier.
Like fish eggs amphibian eggs have no protective shell.
They can only develop in moisture of some kind
and amphibians no matter where they live
must find ways to provide that.
The alpine newt lives on land for about half the year
hunting for slugs and worms.
In winter they lie dormant beneath the snow
but come the spring they get the urge to breed.
A female is swollen with eggs and needs to lay
so she has to go back to water.
And there a male is awaiting her.
He has already developed his breeding colours
and knows how to flaunt them to impress her.
He wafts a pheromone a sexual stimulant
towards her with beats of his tail.
She senses it through her nostrils.
She tastes it in her mouth.
Having caught her interest he turns and moves away from her.
His genital opening is greatly swollen and from it comes a small white capsule.
It is a packet of sperm.
The female led by the male walks directly over it.
He stops and so does she
with her genital opening exactly above the sperm packet
and she picks it up.
So as in many fish
mating occurs with little or no physical contact
between the two partners.
Two or three days later she begins to lay.
Each of her eggs is deposited individually.
As an egg emerges
she wraps the leaf around it with her hind legs
and then holds it there while the edges bond.
She will lay several eggs a day for week after week until eventually
she may have produced several hundred.
But all this has to be done in water.
She has still not broken her link with her fishy ancestry.
In North America in the eastern half of the country
there are many kinds of small salamanders only a few inches long
that have taken one further step away from the aquatic life.
In spring the woodlands are drenched in rain
and suddenly in response
an amphibian army appears among the leaf litter.
Marbled salamanders.
First to emerge are the males. Theyre in search of females.
They have spent the winter deep in the damp leaf litter
breathing by absorbing oxygen from the air
through their moist skins.
For them the land is truly home.
If they were submerged in water for any length of time
they might well drown.
Nonetheless their courtship techniques are much the same
as those used in water by newts.
The males produce pheromones that excite the females.
They deposit capsules of sperm on the damp ground
and the females crawl over them and take them in.
In due course each female lays her soft-skinned eggs on the ground
and stays beside them on guard.
Here its damp enough to prevent her eggs from drying
and theyre already developing rapidly.
Eventually the continuing rains flood the woodland floor.
But now the females needs and those of her eggs are exactly opposite.
They will need water in order to breathe
but she could drown in it so she has to leave.
The young inside their capsules are developing into creatures
fundamentally different from their parents.
A form that is characteristic of amphibians.
They are becoming tadpoles.
They swim free equipped with feathery gills
that enable them to extract oxygen from the water.
They are truly aquatic creatures.
But they have front legs as well as gills.
And within days they develop back legs as well.
As time passes they grow stronger.
Their gills wither and disappear and at last
they are miniature versions of their parents
and are ready to leave the water forever
and to start on their land-living lives.
But what tempted those ancient fish to leave the water in the first place?
Food.
When the first amphibians moved out of water
the land was already swarming with insects.
And the amphibians have evolved a special weapon
with which to catch them.
Salamanders however have not yet developed the athleticism needed
for a high-speed chase and a lightning pounce.
Their hunts are rather solemn sedate affairs.
A simple contraction of the muscles surrounding the tongue
is all thats needed to shoot it forward.
Some salamanders have a tongue
that is about three-quarters the length of the body
but most species have to get pretty close to their prey
if they are to catch it.
Although the adult marbled salamander lives entirely on land
it nonetheless needed water at the very beginning of its life.
But there are other species of salamander in North America
that have managed to break even that link with their distant aquatic past.
This is a gold mine.
The people who dug it found nothing
but biologists who came later found gold of their own special kind.
They discovered a colony of a species called the slimy salamander
that could be properly observed
throughout the summer when normally they are hidden in the leaf litter.
They were all females
and their behaviour proved to be very surprising indeed.
These salamanders come down in early summer in about June
and will travel several hundred metres down along this mine shaft
to exactly the same ledge
within an inch or so that they used the previous year.
And they have been seen doing that for at least five or six years.
And they dont eat.
They will stay down here for six or seven months
sustained only by the food reserves
that theyve accumulated in their fat tails.
Down here
there is permanent moisture however hot and dry it gets outside.
The salamanders clearly prefer to cluster together
close to one another
for the rock walls of the mine shaft elsewhere
are totally uninhabited.
However this open plan way of life while its clearly very successful
nonetheless comes at a price.
Some of the females here are up to no good.
They failed to fatten up enough during the spring
and theyre hungry and in search of a good meal.
And the eggs and young of the other salamanders
will do very well.
To see exactly what these creatures are doing
we need to turn off our torches and turn on the infrared camera.
Here comes one of those marauding females.
She must have located this mother guarding her eggs by smell
for all this is going on in total darkness.
So some amphibians when needs be are neither sluggish insensitive
nor lacking in maternal concern.
And mother wins the day.
The salamanders need to keep moist
means that they seldom come out into the open
but find their prey by pushing through the leaf litter.
And to do that it helps to be slim.
Very slim.
Legs are less in the way if theyre small.
And one great group of burrowing amphibians
has lost its legs altogether.
You might think that this was a giant earthworm
but if you picked it up
you would immediately realise it has got a strong firm backbone.
Its a caecilian.
Caecilians are found in almost all rainforests.
But they are seldom seen
for they spend nearly all their lives underground.
The female having produced her young
stays in her nest chamber to protect them.
Caecilian eyes are rudimentary.
Theyre covered in skin and scarcely function.
In the darkness underground however
the animals have no need for them.
The young enthusiastically lick a secretion from a gland
at the end of their mothers tail
and their constant hunger seems to be
the factor that keeps this little blind family together.
In a single week the young incredibly increase their weight by 1 0 times
apparently just from drinking her secretion.
But could that be their only food?
As we filmed
one of the youngsters revealed a clue to their rapid growth.
It yawned.
It already had hooked teeth like a baby shark.
It surely doesnt need these if its going to do nothing but drinking.
Could it be feeding on something else?
A few hours later our cameras for the first time revealed the answer.
There was a sudden frenzy of activity.
The babies started swarming all over their mother.
They were tearing at her flanks ripping off segments of her skin.
Skin that proved to be full of fat.
It turned out that she regrew her skin every three days
to provide her young with another nourishing meal.
Blind elongated and legless caecilians maybe
but simple inoffensive earthworms they are not.
The most numerous and successful of all amphibians however
have kept their legs and developed them spectacularly.
Some are walkers.
Others are climbers.
There are hoppers.
There are even gliders
who use the membranes on their feet like parachutes.
If their skin is very moist we call these creatures frogs.
If its less so we call them toads.
But they all belong to the same group.
There are some 2200 different kinds of frogs and toads
in the world today
and here in the leaf litter in this Madagascan forest
is the tiniest of them all.
This is fully adult and in its tiny body
which is only a centimetre long
is packed a beating heart a skeleton a gut a brain.
Its a miracle of miniaturisation.
And this basic body plan not only comes in all sizes
but many different shapes which has enabled frogs and toads
to colonise all kinds of different environments.
Out of water frogs found a new way to communicate with one another.
(CROAKING)
Amphibian lungs are comparatively feeble
so frogs amplify their calls with cheek or throat pouches
which act as resonators.
The call of a frog in this South African pool can be heard over a mile away.
(HIGH-PITCHED CROAKING)
Its the painted reed frog the loudest caller of all for his size.
(CROAKING)
But a female is not only impressed by the loudness of a males call
she also judges him by how frequently he manages to make that call.
(CROAKING RAPIDLY)
Calling is a very demanding activity
requiring a male to increase his energy consumption by about 20 times.
So in picking the loudest and fastest caller
the female is also selecting the fittest and most vigorous male
as the father of her offspring.
Hes the one.
Success.
And silence for a few minutes.
In some circumstances however calls need reinforcing with gestures.
The sound of rushing water could drown out the calls of a frog.
However here in this stream in Panama theres a species living alongside
that has developed a novel way of dealing with that problem.
The rare and wonderful golden frog.
It does have a voice but its not loud.
(CROAKS)
Individual males set up their territories beside the river
and then wait for females to turn up.
And since good positions in the territory are not common
they may have to hold them against intruders.
And here one comes.
just in case his call is inaudible he makes his message clear with a wave.
And his rival waves back.
He repeats his message so theres no misunderstanding.
But rival is not deterred.
Well that makes things perfectly clear.
Another arrives. Perhaps at last this is a female.
No its another male.
So there will have to be a wrestling match.
(CROAKS)
That should teach him.
And his rival signals submission by keeping his head down.
(CROAKS)
Now where are those females?
And here she is.
She is pure unblemished gold and much bigger than he is.
While he is fully occupied another challenger arrives.
Since hes already in position
there is no point in breaking away for another wrestling match
so he hangs on.
The golden frog has a powerful poison in its skin
so it can afford to be conspicuous.
But most frogs find safety in camouflage.
This is a South American red-eyed tree frog
a close match for the leaves on which it habitually sits.
The eggs are not very conspicuous either
just little blobs in transparent jelly.
And theyre always laid over water.
They develop very rapidly.
In less than a week they have become recognisable tadpoles
almost ready for freedom.
Then the jelly liquefies
and they simply drop into the water beneath.
But some dont survive long enough to do so.
Wasps raid the cluster
and carry off the unhatched tadpoles to feed their young.
But the tadpoles are not entirely helpless.
By the time they are five days old they know when they are under attack.
And whats more they can do something about it.
There.
Quick wriggle and the tadpole drops to safety.
The alarm spreads quickly through the whole cluster
and they all take a dive.
Their tails are not yet fully developed but they can swim well enough
to take refuge beneath the leaves of the water plants.
So if theres a choice between being carried off by a wasp
and taking an early bath theres no competition.
But not all frogs abandon their young.
If you are big enough you can stay and defend them.
And the male giant African bullfrog is as big as a football.
His pool which formed during the rainy season
lies near the margin of a much bigger pond.
The nursery pool was a good place to lay
for it had none of the predators that abound in the bigger permanent pond.
But as the dry season warms up that smaller pool begins to evaporate.
The tadpoles are now in real danger.
Father takes action.
He starts to dig a canal
to enable his endangered tadpoles to reach the deeper pond nearby.
It will be touch and go but if they can only get to the bigger pond
they are now vigorous enough to have a reasonable chance of survival.
Breakthrough.
And father leads the way.
In the rain forests of South America the daily rains create a multitude
of tiny pools in the centre of many plants.
This tiny poison-arrow frog is carrying his tadpole pig-a-back.
It hatched on a leaf
and now hes taking it to a pool in a bromeliad
high up in the branches.
The tadpole wriggles off.
He may have half a dozen babies each of which he puts into its own tiny pool.
He makes regular tours of all his nurseries
checking on his tadpoles welfare.
This youngster is hungry and tells him so by nibbling his legs
and vibrating against his body.
But the male cant feed the tadpole himself. He needs help.
He has to find a female.
(CROAKING)
There she is.
He calls.
(CROAKING)
And she follows.
He has to lead for only he knows exactly where he deposited each tadpole.
This one is now very hungry indeed.
He calls to the female encouragingly.
(CROAKING)
She jumps in perhaps to assess the situation.
Out she comes without having done whats required so he keeps calling.
(CONTINUES CROAKING)
In she goes a second time.
This time she produces food for the hungry tadpole an infertile egg.
There.
Out she comes and mother and father embrace.
Baby has its dinner.
Australia in the southeast has temperate rainforests.
A cluster of frogs eggs on the damp ground.
When these hatch the tadpoles will also need a moist nursery.
Father a marsupial frog is on guard.
The eggs are developing fast.
The male has to keep a careful eye on them
for he must be close beside them at the very moment when they hatch.
Its going to be a long wait at least 1 1 days.
He seems to have decided that the crucial moment has arrived
and lowers himself onto the eggs.
As he does so the tough egg membranes liquefy
and the young wriggle free.
He has two pouches in his skin one on each hip
and the tadpoles start to squirm into them.
Competition between the tadpoles is intense
for there are more of them than he can accommodate in his pouches.
At last hes taken on board as many as he can manage.
He will now look after them for up to six weeks.
The young remain in his pouches continuing their development
fuelled by the remains of the yolk in their infant stomachs.
And then one night his behaviour changes.
His flanks are rippling.
The first of his young is emerging.
The profound transformation that converted a tadpole into this young frog
took place entirely within its fathers moist pouch.
The parched bush country of Southern Africa.
Here it rains only twice a year and then only briefly.
But when it does the ground in places erupts.
Rain frogs as they are aptly called
have been waiting for months below ground for this moment.
After starving for so long they are keen to feed.
As darkness falls the males begin to call.
Females are fat with eggs.
The males are so much smaller that they cant embrace a female.
So they produce glue from glands on their underside
and stick themselves to their partners back.
But sometimes that only results in a chain of enthusiastic
but undiscriminating males stuck to one another.
Their brief time above ground has come to an end.
The female starts to dig.
The diminutive male being stuck on goes with her.
He will fertilise the eggs later below ground.
Her stay on the surface is over.
The female has excavated a little chamber for herself
and below that she has made a second one
which she has filled with a frothy foam.
This is the nursery for her tadpoles.
The female stays underground away from the lethal heat for several more weeks.
By now her offspring have almost completed their time as tadpoles.
The rains return.
Below ground the youngsters await their release.
The female leads the way
and her brood are with her.
Rain is even rarer in Australia.
There in the central deserts it may not fall for years on end.
But there are amphibians even here
little toads that remain underground in a state of suspended animation
for years just to take advantage of a few rainy days.
After the rains have fallen spadefoot toads all emerge together.
They must feed and breed if possible before the sun rises.
But the desert dries only too quickly even after the heaviest of storms.
Temperatures rise to 20 degrees centigrade.
Now water will evaporate instantly.
This is one of the hottest places on Earth.
So the toads have to retreat once again below ground.
The miracle is that theyre here at all.
A toad that can live in as parched a desert as this
is impressive evidence of the versatility of the amphibians
the way they can adapt their behaviour and their anatomy
to live so far away from water.
But there is one group of animals that can really call the desert their own.
The lizards.
And well look at them in the next episode of Life in Cold Blood.
Amphibians are the most threatened group of vertebrates on the planet.
In recent years a strange and lethal fungal disease
has started to spread among them.
The golden frog which lives only in one small area in Panama
was in particular danger
as the disease is already on the frontier of its territory.
If we were to film it at all we would have to move quickly.
For series producer Miles Barton
that meant mean cutting short Christmas.
(PLANE ENGINE WHIRRING)
We had been told that in Panama
the frogs few remaining breeding streams
were being rapidly destroyed by the building of a new road
making the last tiny population even more at risk from the disease.
The fungus clogs the animals moist skin.
Since all frogs breathe through their skin
infected animals die from suffocation.
Frog biologist Erik Lindquist
who first described the golden frogs signalling behaviour
helped the film team to thoroughly disinfect their kit
before travelling into the frogs territory.
Freshly scrubbed up Erik took the team
to one of the golden frogs last known breeding sites.
But would they still be there?
(CROAKING)
Yeah you hear that? Thats a male calling.
Okay we have another male crawling up over here
crawling up the rock face.
ATTENBOROUGH: But with the fungus approaching at a rate of up to
22 miles a year
the frogs were rapidly disappearing from all their known breeding sites.
The advance crew immediately set about filming
as much of the behaviour as they could.
By the time I arrived
there was only one remaining location where the frogs survived.
Where exactly are we going?
I would prefer not saying precisely.
You see this is really the last population of the golden frog
left in the wild.
And historically the locals have been collecting out these animals
as good-luck talismans.
And so now left with just one population
Im concerned that if this secret locality gets given out
there will be international collectors that would come.
ATTENBOROUGH: Really?
Sure. Theyre rare enough now
where many people would pay top dollar for these animals.
Were they ever what you might call common?
When I talked to people who had been here in the past
the populations were so abundant that one would have to watch
where theyre stepping to keep from killing one.
-Really? -Yes.
Erik has his own low-tech method of finding them
which he assures me normally works.
(IMITATING CROAKING)
See when you call sometimes theyll call back
and theyll reveal their location.
Sometimes theyre tucked away behind leaves
and theyre really difficult to find.
Hopefully we can elicit a response.
(IMITATING CROAKING)
Its the fastest way to get them to shut up.
(CROAKING)
-Was that him? -Yeah. Listen.
(CROAKING)
-So theyre here. -Theyre here. Theres one over here.
-LINDQUIST: See him right there. -Yeah yeah.
LINDQUIST: Looks like a male.
Make him do it again.
(IMITATING CROAKING)
(CROAKING)
(GRUNTING)
You have to hum and whistle at the same time.
Cant do it. See if he can.
(LINDQUIST IMITATING CROAKING)
(ATTENBOROUGH GRUNTING)
(LINDQUIST IMITATING CROAKING)
(CHUCKLING)
Now we knew the frogs were still here we could complete the filming.
The local people have always treasured their remarkable little frog
but Erik was the first to document its signalling behaviour.
It was an animal that was just walking.
I wasnt sure if the animal was trying to flush out prey
or if it was using it in a communication role.
And so a group of us set out to look at whether or not this was communication.
We tried mirror presentations to the animals.
And when you presented them with a mirror
they would hand wave at the mirror as opposed to say
maybe the backside of a mirror that didnt have a reflective surface.
Some of us have looked specifically at an LCD screen
a little television with a hand-waving semaphoring frog
and its elicited a number of responses specifically from males.
ATTENBOROUGH: You show a television picture to a male and he waves back?
-He waves back and hell even call... -Really?
...to the male on the television screen.
-Its really fascinating. -Yes. Absolutely.
They then experimented with a life-size plastic model
complete with waving arm
the sort of high-tech gear I thought I might manage to operate myself.
Its not as easy as you might think.
Erik showed me how it should be done.
Youve got to get that slow-motion wave just right.
The frogs waved.
They called.
(CROAKING)
They even attacked.
So that wave really is a form of communication.
So theyre just saying Keep off keep off.
Is that right?
Were not sure. Sometimes there seem to be certain hand waves
that may indicate appeasement showing that
Im just walking through perhaps your territory. Dont bother me.
Really? Ah please.
(ATTENBOROUGH LAUGHING)
But how endangered is the golden frog?
This is it what you see.
Youre going to be the last crew to film these in the wild.
And indeed we were. Soon after finishing filming
the local scientists decided the time had come
to take all the surviving golden frogs into captivity
before the fungus arrives here and kills them all.
They and other rare species of frog also threatened
were being brought back to a special frog hospital
where I was introduced to some of the other patients.
-So what are these? -Theyre nocturnal also...
ATTENBOROUGH: Here theyre being treated daily with a fungicide
but without a vaccine to protect them
and with the fungus still at large in the forest
they cant be reintroduced into their proper home.
Frogs so common in these humid forests are crucial links in the ecology.
If they disappear all kinds of food chains will be broken
and the effect could be little short of catastrophic to wildlife in general.
And sadly for now at least
it seems that the golden frog has waved its last in the wild.