Land Invaders Life in Cold Blood

Amphibians were the first backboned animals to leave the water

and colonise the land.

Today there are some 6,000 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 AND CHIRRUPING

Choruses like this ensure that we are well aware of frogs and toads.

But there are other kinds of amphibians

that don't 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?

400 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

managed to survive,

because it has a rare talent for a fish -

it has lungs and can breathe air.

And there's 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.

It's 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 riverbanks,

and defend them against all other males.

A newcomer arrives, looking for a breeding den of his own.

It won't be here.

The resident male has good reason to be so defensive.

He's 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 it.

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's 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.

They're 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, it's damp enough to prevent her eggs from drying,

and they're already developing rapidly.

Eventually, the continuing rains flood the woodland floor.

But now the female's 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're 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 that's needed to shoot it forward.

Some salamanders have a tongue that is about three-quarters

the length of their body, but most species

have to get pretty close to their prey if they're 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're 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 mineshaft

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 don't eat.

They will stay down here for six or seven months,

sustained only by the food reserves

that they've 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 mineshaft elsewhere are totally uninhabited.

However, this open-plan way of life,

while it's 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 they're hungry and in search of a good meal.

And the eggs and young of their 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 they're 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's got a strong, firm backbone.

It's 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.

They're 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 mother's 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 ten 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 hook teeth like a baby shark.

It surely doesn't need these if it's 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 may be,

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 it's less so, we call them toads,

but they all belong to the same group.

There are some 5,500 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.

It's 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.

It's the painted reed frog, the loudest caller of all, for his size.

But a female is not only impressed by the loudness of a male's call.

She also judges him

by how frequently he manages to make that call.

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.

He's 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,

there's 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 it's not loud.

Individual males set up their territories beside the river,

and then wait for females to turn up.

And since good positions for a 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 there's no misunderstanding.

But rival is not deterred.

Well, that makes things perfectly clear.

Another arrives.

Perhaps, at last, this is a female.

No, it's another male, so there will have to be a wrestling match.

That should teach him.

His rival signals submission by keeping his head down.

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 he's already in position,

there's 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 they're always laid over water.

They develop very rapidly.

In less than a week, they've become recognisable tadpoles,

almost ready for freedom.

Then the jelly liquefies and they simply drop into the water beneath.

But some don't 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're five days old, they know when they're under attack,

and, what's 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 there's a choice between being carried off by a wasp

and taking an early bath, there's no competition.

But not all frogs abandon their young.

If you're 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.

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're now vigorous enough to have a reasonable chance of survival.

Breakthrough.

And Father leads the way.

In the rainforests 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 piggy-back.

It hatched on a leaf and now he's 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 can't feed the tadpole himself - he needs help.

He has to find a female.

There she is.

He calls.

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.

She jumps in, perhaps to assess the situation.

Out she comes,

without having done what's required, so he keeps calling.

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 south-east, 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.

It's going to be a long wait.

At least 11 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, he's 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 father's 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're aptly called,

have been waiting for months below ground for this moment.

After starving for so long, they're keen to feed.

As darkness falls, the males begin to call.

HIGH-PITCHED CHIRRUP

Females are fat with eggs.

The males are so much smaller that they can't embrace a female,

so they produce glue from glands on their underside,

and stick themselves to their partner's 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's made a second one,

which she's 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 50 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 they're 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's one group of animals

that can really call the desert their own - the lizards.

And we'll 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 cutting short Christmas.

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 animal's moist skin.

Since all frogs breathe through their skin,

infected animals die from suffocation.

Frog biologist Erik Lindquist,

who first described the golden frog's 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 frog's last-known breeding sites.

But would they still be there?

DISTANT CROAK

Yeah, you hear that? That's a male calling.

We have another male crawling up over here,

crawling up the rock face.

But with the fungus approaching at a rate of up to 25 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 talisman, and so now we're left with just one population.

I'm concerned that if the secret locality gets given out,

-there'll be international collectors that would come.

-Really?

Sure. They're rare enough now

where many people would pay top dollar for these animals.

Were they ever what you might call common?

When I talk to people who have been here in the past,

the populations were so abundant that one would have to watch where they're

stepping to keep from killing one.

-Really?

-Yes, yes.

Erik has his own low-tech method of finding them,

which he assures me normally works.

LOW WHISTLING

See, when you call, sometimes they'll call back

and they'll reveal their locations.

Sometimes they're tucked away behind leaves

and they're really difficult to find.

Hopefully we can elicit a response.

HE WHISTLES

It's the fastest way to get them to shut up.

-Was that him?

-Yeah, listen.

-So they're here?

-They're here.

There's one over there.

See him right there. Looks like a male.

Make him do it again.

HE WHISTLES

FROG WHISTLES

-You have to hum and whistle at the same time.

-Can't do it!

See if he can.

HE TRIES TO WHISTLE

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 wasn't 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.

When you presented them with a mirror,

they would hand-wave at the mirror

as opposed to, say, the backside of a mirror that wasn't reflective.

Some of us have looked specifically at an LCD screen,

a little television with a hand-waving, semaphoring frog,

and it has elicited a number of responses, specifically from males.

What, you show a television picture to a male and he waves back?

He waves back and he'll even call, to the male on the television screen.

-Really?

-It's really fascinating.

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.

It's not as easy as you might think.

Erik showed me how it should be done.

You've got to get that slow-motion wave just right.

The frogs waved.

They called.

They even attacked.

So that wave really is a form of communication.

So they're just saying, "Keep off, keep off."

Huh, is that right?

We're not sure. Sometimes there seem to be certain hand waves

that may indicate appeasement,

showing that, "I'm just walking through, perhaps, your territory.

"Don't bother me."

Really? "Ah, please."

But how endangered is the golden frog?

This is it. What you see.

You're 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?

They're nocturnal, so they spend...

'Here, they're being treated daily with a fungicide.

'But without a vaccine to protect them,

'and with the fungus still at large in the forest,

'they can't be re-introduced 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.

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.

Subtitles by Red Bee Media Ltd

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