0:00:44 > 0:00:50Amphibians were the first backboned animals to leave the water
0:00:50 > 0:00:51and colonise the land.
0:00:51 > 0:00:55Today there are some 6,000 species of them,
0:00:55 > 0:00:58and new ones are constantly being discovered.
0:00:58 > 0:01:00We may not often see them,
0:01:00 > 0:01:03but during the breeding season, we certainly hear them.
0:01:03 > 0:01:05CROAKING AND CHIRRUPING
0:01:14 > 0:01:19Choruses like this ensure that we are well aware of frogs and toads.
0:01:26 > 0:01:29But there are other kinds of amphibians
0:01:29 > 0:01:31that don't make themselves so obvious.
0:01:31 > 0:01:36Newts and their close relatives, the salamanders.
0:01:37 > 0:01:41And even ones that have completely lost their legs.
0:01:43 > 0:01:47But all amphibians have one thing in common - a moist skin.
0:01:47 > 0:01:49If that dries, they die.
0:01:51 > 0:01:55And dealing with that danger dominates their lives.
0:01:55 > 0:01:58How are they to survive away from water?
0:02:06 > 0:02:09400 million years ago,
0:02:09 > 0:02:12the only backboned animals on the Earth were fish.
0:02:12 > 0:02:16The land was empty, except for insects and other invertebrates.
0:02:16 > 0:02:21But then, one of those fish managed to haul itself out of the water
0:02:21 > 0:02:23and up on to the land.
0:02:23 > 0:02:26You can see what sort of creature that might have been
0:02:26 > 0:02:29if you go to north-east Australia.
0:02:29 > 0:02:31There, the rivers only too often dry up.
0:02:34 > 0:02:39But one remarkable, ancient and extraordinary fish
0:02:39 > 0:02:41managed to survive,
0:02:41 > 0:02:44because it has a rare talent for a fish -
0:02:44 > 0:02:48it has lungs and can breathe air.
0:02:48 > 0:02:50And there's one at my feet, right here.
0:02:52 > 0:02:56Fossils just like it date from precisely the time
0:02:56 > 0:02:59when the great invasion of the land took place.
0:02:59 > 0:03:03On occasion, it rises to the surface and gulps air.
0:03:06 > 0:03:09The air goes into a pouch that opens from its throat,
0:03:09 > 0:03:12where the oxygen from it is absorbed.
0:03:12 > 0:03:15This is a lungfish.
0:03:18 > 0:03:21It punts itself along the river bottom,
0:03:21 > 0:03:26using two pairs of fleshy, muscular fins placed low on its body
0:03:26 > 0:03:28just like simple legs.
0:03:30 > 0:03:36Sometime around 360 million years ago, one of its remote ancestors
0:03:36 > 0:03:42used such limb-like fins to push itself up onto the land.
0:03:47 > 0:03:52That pioneer may have looked much like this strange monster
0:03:52 > 0:03:55that haunts the waterways of Japan.
0:03:58 > 0:04:02It's the giant salamander, the biggest of all living amphibians,
0:04:02 > 0:04:06that grows to a metre or more in length.
0:04:11 > 0:04:15It, too, has lungs and breathes air.
0:04:15 > 0:04:19But even so, it almost never leaves the water.
0:04:21 > 0:04:25Males make their dens in both natural and man-made retreats
0:04:25 > 0:04:26in the riverbanks,
0:04:26 > 0:04:29and defend them against all other males.
0:04:30 > 0:04:35A newcomer arrives, looking for a breeding den of his own.
0:05:10 > 0:05:11It won't be here.
0:05:18 > 0:05:22The resident male has good reason to be so defensive.
0:05:25 > 0:05:27He's guarding a batch of eggs,
0:05:27 > 0:05:32left by a female who visited him a few days earlier.
0:05:32 > 0:05:36Like fish eggs, amphibian eggs have no protective shell.
0:05:36 > 0:05:38They can only develop in moisture of some kind,
0:05:38 > 0:05:43and amphibians, no matter where they live, must find ways to provide it.
0:05:46 > 0:05:50The alpine newt lives on land for about half the year,
0:05:50 > 0:05:52hunting for slugs and worms.
0:05:54 > 0:05:57In winter, they lie dormant beneath the snow,
0:05:57 > 0:06:00but come the spring, they get the urge to breed.
0:06:05 > 0:06:09A female is swollen with eggs and needs to lay,
0:06:09 > 0:06:12so she has to go back to water.
0:06:18 > 0:06:22And there, a male is awaiting her.
0:06:22 > 0:06:26He has already developed his breeding colours
0:06:26 > 0:06:29and knows how to flaunt them to impress her.
0:06:34 > 0:06:36He wafts a pheromone, a sexual stimulant,
0:06:36 > 0:06:39towards her with beats of his tail.
0:06:52 > 0:06:55She senses it through her nostrils.
0:07:05 > 0:07:08She tastes it in her mouth.
0:07:14 > 0:07:19Having caught her interest, he turns and moves away from her.
0:07:21 > 0:07:23His genital opening is greatly swollen,
0:07:23 > 0:07:26and from it comes a small white capsule.
0:07:26 > 0:07:29It's a packet of sperm.
0:07:32 > 0:07:38The female, led by the male, walks directly over it.
0:07:38 > 0:07:41He stops and so does she,
0:07:41 > 0:07:45with her genital opening exactly above the sperm packet,
0:07:45 > 0:07:47and she picks it up.
0:07:53 > 0:07:58So, as in many fish, mating occurs with little or no physical contact
0:07:58 > 0:08:01between the two partners.
0:08:03 > 0:08:07Two or three days later, she begins to lay.
0:08:12 > 0:08:16Each of her eggs is deposited individually.
0:08:27 > 0:08:31As an egg emerges, she wraps the leaf around it with her hind legs,
0:08:31 > 0:08:34and then holds it there while the edges bond.
0:08:36 > 0:08:40She will lay several eggs a day for week after week,
0:08:40 > 0:08:44until, eventually, she may have produced several hundred.
0:08:49 > 0:08:52But all this has to be done in water.
0:08:52 > 0:08:57She has still not broken her link with her fishy ancestry.
0:08:59 > 0:09:03In North America, in the eastern half of the country,
0:09:03 > 0:09:07there are many kinds of small salamanders, only a few inches long,
0:09:07 > 0:09:12that have taken one further step away from the aquatic life.
0:09:14 > 0:09:19In spring, the woodlands are drenched in rain,
0:09:19 > 0:09:20and suddenly, in response,
0:09:20 > 0:09:23an amphibian army appears among the leaf litter.
0:09:26 > 0:09:28Marbled salamanders.
0:09:31 > 0:09:34First to emerge are the males.
0:09:34 > 0:09:36They're in search of females.
0:09:37 > 0:09:40They have spent the winter deep in the damp leaf litter,
0:09:40 > 0:09:45breathing by absorbing oxygen from the air, through their moist skins.
0:09:45 > 0:09:48For them, the land is truly home.
0:09:48 > 0:09:51If they were submerged in water for any length of time,
0:09:51 > 0:09:54they might well drown.
0:09:55 > 0:09:59Nonetheless, their courtship techniques are much the same
0:09:59 > 0:10:02as those used in water by newts.
0:10:06 > 0:10:10The males produce pheromones that excite the females.
0:10:17 > 0:10:22They deposit capsules of sperm on the damp ground.
0:10:22 > 0:10:27And the females crawl over them and take them in.
0:10:28 > 0:10:33In due course, each female lays her soft-skinned eggs on the ground,
0:10:33 > 0:10:36and stays beside them, on guard.
0:10:37 > 0:10:41Here, it's damp enough to prevent her eggs from drying,
0:10:41 > 0:10:44and they're already developing rapidly.
0:10:50 > 0:10:55Eventually, the continuing rains flood the woodland floor.
0:10:57 > 0:11:01But now the female's needs and those of her eggs are exactly opposite.
0:11:01 > 0:11:05They will need water in order to breathe,
0:11:05 > 0:11:08but she could drown in it, so she has to leave.
0:11:13 > 0:11:17The young inside their capsules are developing into creatures
0:11:17 > 0:11:20fundamentally different from their parents,
0:11:20 > 0:11:23a form that is characteristic of amphibians.
0:11:23 > 0:11:25They are becoming tadpoles.
0:11:27 > 0:11:31They swim free, equipped with feathery gills that enable them
0:11:31 > 0:11:33to extract oxygen from the water.
0:11:33 > 0:11:36They are truly aquatic creatures...
0:11:38 > 0:11:42..but they have front legs as well as gills.
0:11:49 > 0:11:53And within days, they develop back legs as well.
0:11:56 > 0:11:58As time passes, they grow stronger.
0:11:58 > 0:12:01Their gills wither and disappear,
0:12:01 > 0:12:04and at last, they're miniature versions of their parents,
0:12:04 > 0:12:07and are ready to leave the water forever,
0:12:07 > 0:12:10and to start on their land-living lives.
0:12:10 > 0:12:15But what tempted those ancient fish to leave the water
0:12:15 > 0:12:17in the first place?
0:12:17 > 0:12:19Food.
0:12:20 > 0:12:23When the first amphibians moved out of water,
0:12:23 > 0:12:26the land was already swarming with insects.
0:12:26 > 0:12:30And the amphibians have evolved a special weapon
0:12:30 > 0:12:31with which to catch them.
0:12:39 > 0:12:43Salamanders, however, have not yet developed the athleticism
0:12:43 > 0:12:47needed for a high-speed chase and a lightning pounce.
0:12:47 > 0:12:51Their hunts are rather solemn, sedate affairs.
0:13:12 > 0:13:16A simple contraction of the muscles surrounding the tongue
0:13:16 > 0:13:18is all that's needed to shoot it forward.
0:13:23 > 0:13:27Some salamanders have a tongue that is about three-quarters
0:13:27 > 0:13:30the length of their body, but most species
0:13:30 > 0:13:33have to get pretty close to their prey if they're to catch it.
0:13:40 > 0:13:44Although the adult marbled salamander lives entirely on land,
0:13:44 > 0:13:48it nonetheless needed water at the very beginning of its life.
0:13:48 > 0:13:52But there are other species of salamander in North America
0:13:52 > 0:13:54that have managed to break even that link
0:13:54 > 0:13:56with their distant aquatic past.
0:14:03 > 0:14:06This is a gold mine.
0:14:06 > 0:14:08The people who dug it found nothing.
0:14:08 > 0:14:11But biologists, who came later,
0:14:11 > 0:14:14found gold of their own special kind.
0:14:23 > 0:14:27They discovered a colony of a species called the slimy salamander,
0:14:27 > 0:14:30that could be properly observed throughout the summer,
0:14:30 > 0:14:32when normally they're hidden in the leaf litter.
0:14:32 > 0:14:34They were all females,
0:14:34 > 0:14:38and their behaviour proved to be very surprising indeed.
0:14:43 > 0:14:49These salamanders come down in early summer, in about June,
0:14:49 > 0:14:55and will travel several hundred metres down along this mineshaft
0:14:55 > 0:14:59to exactly the same ledge, within an inch or so,
0:14:59 > 0:15:02that they used the previous year.
0:15:02 > 0:15:08And they have been seen doing that for at least five or six years.
0:15:08 > 0:15:10And they don't eat.
0:15:10 > 0:15:13They will stay down here for six or seven months,
0:15:13 > 0:15:16sustained only by the food reserves
0:15:16 > 0:15:20that they've accumulated in their fat tails.
0:15:22 > 0:15:25Down here there is permanent moisture,
0:15:25 > 0:15:27however hot and dry it gets outside.
0:15:30 > 0:15:33The salamanders clearly prefer to cluster together,
0:15:33 > 0:15:35close to one another,
0:15:35 > 0:15:39for the rock walls of the mineshaft elsewhere are totally uninhabited.
0:15:41 > 0:15:45However, this open-plan way of life,
0:15:45 > 0:15:47while it's clearly very successful,
0:15:47 > 0:15:50nonetheless comes at a price.
0:15:51 > 0:15:55Some of the females here are up to no good.
0:15:55 > 0:15:58They failed to fatten up enough during the spring,
0:15:58 > 0:16:03and they're hungry and in search of a good meal.
0:16:03 > 0:16:08And the eggs and young of their other salamanders
0:16:08 > 0:16:10will do very well.
0:16:11 > 0:16:14To see exactly what these creatures are doing,
0:16:14 > 0:16:19we need to turn off our torches and turn on the infrared camera.
0:16:27 > 0:16:30Here comes one of those marauding females.
0:16:40 > 0:16:45She must have located this mother, guarding her eggs, by smell,
0:16:45 > 0:16:48for all this is going on in total darkness.
0:17:07 > 0:17:09So some amphibians, when needs be,
0:17:09 > 0:17:15are neither sluggish, insensitive nor lacking in maternal concern.
0:17:20 > 0:17:22And mother wins the day.
0:17:26 > 0:17:28The salamanders' need to keep moist
0:17:28 > 0:17:31means that they seldom come out into the open,
0:17:31 > 0:17:35but find their prey by pushing through the leaf litter.
0:17:35 > 0:17:38And to do that, it helps to be slim.
0:17:38 > 0:17:40Very slim.
0:17:40 > 0:17:43Legs are less in the way if they're small.
0:17:46 > 0:17:50And one great group of burrowing amphibians
0:17:50 > 0:17:52has lost its legs altogether.
0:17:57 > 0:18:01You might think that this was a giant earthworm.
0:18:01 > 0:18:03But if you picked it up,
0:18:03 > 0:18:07you would immediately realise it's got a strong, firm backbone.
0:18:07 > 0:18:09It's a caecilian.
0:18:10 > 0:18:15Caecilians are found in almost all rainforests.
0:18:15 > 0:18:17But they are seldom seen,
0:18:17 > 0:18:20for they spend nearly all their lives underground.
0:18:21 > 0:18:24The female, having produced her young,
0:18:24 > 0:18:28stays in her nest chamber to protect them.
0:18:34 > 0:18:36Caecilian eyes are rudimentary.
0:18:36 > 0:18:38They're covered in skin, and scarcely function.
0:18:38 > 0:18:41In the darkness underground, however,
0:18:41 > 0:18:43the animals have no need for them.
0:18:46 > 0:18:50The young enthusiastically lick a secretion from a gland
0:18:50 > 0:18:52at the end of their mother's tail,
0:18:52 > 0:18:55and their constant hunger seems to be the factor
0:18:55 > 0:18:58that keeps this little blind family together.
0:19:06 > 0:19:07In a single week,
0:19:07 > 0:19:12the young, incredibly, increase their weight by ten times,
0:19:12 > 0:19:15apparently just from drinking her secretion.
0:19:15 > 0:19:18But could that be their only food?
0:19:19 > 0:19:22As we filmed, one of the youngsters
0:19:22 > 0:19:25revealed a clue to their rapid growth.
0:19:25 > 0:19:26It yawned.
0:19:28 > 0:19:32It already had hook teeth like a baby shark.
0:19:32 > 0:19:37It surely doesn't need these if it's going to do nothing but drinking.
0:19:37 > 0:19:39Could it be feeding on something else?
0:19:43 > 0:19:48A few hours later, our cameras, for the first time, revealed the answer.
0:19:50 > 0:19:52There was a sudden frenzy of activity.
0:19:52 > 0:19:55The babies started swarming all over their mother.
0:20:07 > 0:20:10They were tearing at her flanks,
0:20:10 > 0:20:12ripping off segments of her skin -
0:20:12 > 0:20:15skin that proved to be full of fat.
0:20:25 > 0:20:30It turned out that she regrew her skin every three days,
0:20:30 > 0:20:33to provide her young with another nourishing meal.
0:20:44 > 0:20:48Blind, elongated and legless caecilians may be,
0:20:48 > 0:20:52but simple, inoffensive earthworms they are not.
0:20:54 > 0:20:59The most numerous and successful of all amphibians, however,
0:20:59 > 0:21:03have kept their legs and developed them spectacularly.
0:21:27 > 0:21:30Some are walkers.
0:21:37 > 0:21:40Others are climbers.
0:21:49 > 0:21:51There are hoppers.
0:21:56 > 0:21:58There are even gliders,
0:21:58 > 0:22:02who use the membranes on their feet like parachutes.
0:22:18 > 0:22:23If their skin is very moist, we call these creatures frogs.
0:22:23 > 0:22:27If it's less so, we call them toads,
0:22:27 > 0:22:29but they all belong to the same group.
0:22:37 > 0:22:42There are some 5,500 different kinds of frogs and toads
0:22:42 > 0:22:45in the world today,
0:22:45 > 0:22:49and here, in the leaf litter in this Madagascan forest,
0:22:49 > 0:22:52is the tiniest of them all.
0:22:52 > 0:22:55This is fully adult,
0:22:55 > 0:22:57and in its tiny body,
0:22:57 > 0:23:00which is only a centimetre long,
0:23:00 > 0:23:02is packed a beating heart,
0:23:02 > 0:23:06a skeleton, a gut, a brain.
0:23:07 > 0:23:10It's a miracle of miniaturisation.
0:23:12 > 0:23:14And this basic body plan
0:23:14 > 0:23:17not only comes in all sizes,
0:23:17 > 0:23:19but many different shapes,
0:23:19 > 0:23:21which has enabled frogs and toads
0:23:21 > 0:23:25to colonise all kinds of different environments.
0:23:27 > 0:23:34Out of water, frogs found a new way to communicate with one another.
0:23:34 > 0:23:36CROAKING
0:23:46 > 0:23:50Amphibian lungs are comparatively feeble,
0:23:50 > 0:23:54so frogs amplify their calls with cheek or throat pouches
0:23:54 > 0:23:55which act as resonators.
0:23:58 > 0:24:01The call of a frog in this South African pool
0:24:01 > 0:24:04can be heard over a mile away.
0:24:07 > 0:24:12It's the painted reed frog, the loudest caller of all, for his size.
0:24:25 > 0:24:30But a female is not only impressed by the loudness of a male's call.
0:24:33 > 0:24:34She also judges him
0:24:34 > 0:24:38by how frequently he manages to make that call.
0:24:50 > 0:24:53Calling is a very demanding activity,
0:24:53 > 0:24:56requiring a male to increase his energy consumption
0:24:56 > 0:24:58by about 20 times,
0:24:58 > 0:25:01so in picking the loudest and fastest caller,
0:25:01 > 0:25:04the female is also selecting the fittest and most vigorous male
0:25:04 > 0:25:07as the father of her offspring.
0:25:16 > 0:25:18He's the one.
0:25:26 > 0:25:29Success, and silence, for a few minutes.
0:25:35 > 0:25:37In some circumstances, however,
0:25:37 > 0:25:40calls need reinforcing with gestures.
0:25:45 > 0:25:51The sound of rushing water could drown out the calls of a frog.
0:25:51 > 0:25:54However, here in this stream in Panama,
0:25:54 > 0:25:57there's a species living alongside
0:25:57 > 0:26:00that has developed a novel way of dealing with that problem.
0:26:02 > 0:26:05The rare and wonderful golden frog.
0:26:05 > 0:26:08It does have a voice, but it's not loud.
0:26:16 > 0:26:20Individual males set up their territories beside the river,
0:26:20 > 0:26:23and then wait for females to turn up.
0:26:23 > 0:26:28And since good positions for a territory are not common,
0:26:28 > 0:26:31they may have to hold them against intruders.
0:26:32 > 0:26:34And here one comes.
0:26:36 > 0:26:39Just in case his call is inaudible,
0:26:39 > 0:26:42he makes his message clear with a wave.
0:26:48 > 0:26:51And his rival waves back.
0:26:53 > 0:26:56He repeats his message so there's no misunderstanding.
0:27:08 > 0:27:10But rival is not deterred.
0:27:11 > 0:27:14Well, that makes things perfectly clear.
0:27:17 > 0:27:19Another arrives.
0:27:19 > 0:27:23Perhaps, at last, this is a female.
0:27:37 > 0:27:41No, it's another male, so there will have to be a wrestling match.
0:27:46 > 0:27:49That should teach him.
0:27:50 > 0:27:55His rival signals submission by keeping his head down.
0:28:21 > 0:28:25Now where are those females?
0:28:28 > 0:28:29And here she is.
0:28:31 > 0:28:35She is pure, unblemished gold and much bigger than he is.
0:28:45 > 0:28:48While he is fully occupied, another challenger arrives.
0:28:53 > 0:28:56Since he's already in position,
0:28:56 > 0:28:59there's no point in breaking away for another wrestling match,
0:28:59 > 0:29:01so he hangs on.
0:29:07 > 0:29:11The golden frog has a powerful poison in its skin,
0:29:11 > 0:29:13so it can afford to be conspicuous,
0:29:13 > 0:29:16but most frogs find safety in camouflage.
0:29:20 > 0:29:25This is a South American red-eyed tree frog,
0:29:25 > 0:29:29a close match for the leaves on which it habitually sits.
0:29:32 > 0:29:36The eggs are not very conspicuous either,
0:29:36 > 0:29:39just little blobs in transparent jelly.
0:29:39 > 0:29:42And they're always laid over water.
0:29:46 > 0:29:49They develop very rapidly.
0:30:09 > 0:30:14In less than a week, they've become recognisable tadpoles,
0:30:14 > 0:30:16almost ready for freedom.
0:30:16 > 0:30:21Then the jelly liquefies and they simply drop into the water beneath.
0:30:23 > 0:30:27But some don't survive long enough to do so.
0:30:31 > 0:30:33Wasps raid the cluster
0:30:33 > 0:30:37and carry off the unhatched tadpoles to feed their young.
0:31:07 > 0:31:10But the tadpoles are not entirely helpless.
0:31:12 > 0:31:16By the time they're five days old, they know when they're under attack,
0:31:16 > 0:31:19and, what's more, they can do something about it.
0:31:21 > 0:31:23There.
0:31:24 > 0:31:28Quick wriggle and the tadpole drops to safety.
0:31:36 > 0:31:40The alarm spreads quickly through the whole cluster,
0:31:40 > 0:31:41and they all take a dive.
0:31:53 > 0:31:56Their tails are not yet fully developed,
0:31:56 > 0:31:59but they can swim well enough to take refuge
0:31:59 > 0:32:01beneath the leaves of the water plants.
0:32:24 > 0:32:28So if there's a choice between being carried off by a wasp
0:32:28 > 0:32:32and taking an early bath, there's no competition.
0:32:33 > 0:32:37But not all frogs abandon their young.
0:32:37 > 0:32:40If you're big enough, you can stay and defend them,
0:32:40 > 0:32:44and the male giant African bullfrog is as big as a football.
0:32:46 > 0:32:49His pool, which formed during the rainy season,
0:32:49 > 0:32:52lies near the margin of a much bigger pond.
0:32:56 > 0:32:58The nursery pool was a good place to lay,
0:32:58 > 0:33:00for it had none of the predators
0:33:00 > 0:33:03that abound in the bigger, permanent pond.
0:33:03 > 0:33:06But as the dry season warms up,
0:33:06 > 0:33:09that smaller pool begins to evaporate.
0:33:11 > 0:33:14Tadpoles are now in real danger.
0:33:16 > 0:33:18Father takes action.
0:33:21 > 0:33:23He starts to dig a canal
0:33:23 > 0:33:27to enable his endangered tadpoles to reach the deeper pond nearby.
0:33:36 > 0:33:40It will be touch and go, but if they can only get to the bigger pond,
0:33:40 > 0:33:45they're now vigorous enough to have a reasonable chance of survival.
0:33:51 > 0:33:53Breakthrough.
0:34:01 > 0:34:04And Father leads the way.
0:34:17 > 0:34:19In the rainforests of South America,
0:34:19 > 0:34:23the daily rains create a multitude of tiny pools
0:34:23 > 0:34:26in the centre of many plants.
0:34:26 > 0:34:32This tiny poison arrow frog is carrying his tadpole piggy-back.
0:34:32 > 0:34:37It hatched on a leaf and now he's taking it to a pool in a bromeliad,
0:34:37 > 0:34:39high up in the branches.
0:34:39 > 0:34:41The tadpole wriggles off.
0:34:43 > 0:34:45He may have half a dozen babies,
0:34:45 > 0:34:49each of which he puts into its own tiny pool.
0:34:56 > 0:34:59He makes regular tours of all his nurseries,
0:34:59 > 0:35:03checking on his tadpoles' welfare.
0:35:09 > 0:35:12This youngster is hungry,
0:35:12 > 0:35:17and tells him so by nibbling his legs and vibrating against his body.
0:35:21 > 0:35:27But the male can't feed the tadpole himself - he needs help.
0:35:37 > 0:35:39He has to find a female.
0:35:47 > 0:35:50There she is.
0:35:54 > 0:35:56He calls.
0:36:05 > 0:36:09And she follows.
0:36:15 > 0:36:17He has to lead,
0:36:17 > 0:36:21for only he knows exactly where he deposited each tadpole.
0:36:23 > 0:36:26This one is now very hungry indeed.
0:36:30 > 0:36:33He calls to the female encouragingly.
0:36:38 > 0:36:43She jumps in, perhaps to assess the situation.
0:36:46 > 0:36:47Out she comes,
0:36:47 > 0:36:51without having done what's required, so he keeps calling.
0:36:51 > 0:36:55In she goes a second time.
0:36:55 > 0:36:59This time she produces food for the hungry tadpole,
0:36:59 > 0:37:01an infertile egg.
0:37:06 > 0:37:07There.
0:37:11 > 0:37:16Out she comes, and mother and father embrace.
0:37:28 > 0:37:32Baby has its dinner.
0:37:42 > 0:37:47Australia, in the south-east, has temperate rainforests.
0:37:48 > 0:37:52A cluster of frogs' eggs on the damp ground.
0:37:52 > 0:37:56When these hatch, the tadpoles will also need a moist nursery.
0:37:56 > 0:38:01Father, a marsupial frog, is on guard.
0:38:01 > 0:38:04The eggs are developing fast.
0:38:09 > 0:38:11The male has to keep a careful eye on them,
0:38:11 > 0:38:16for he must be close beside them at the very moment when they hatch.
0:38:24 > 0:38:26It's going to be a long wait.
0:38:26 > 0:38:29At least 11 days.
0:38:39 > 0:38:43He seems to have decided that the crucial moment has arrived,
0:38:43 > 0:38:47and lowers himself onto the eggs.
0:38:52 > 0:38:55As he does so, the tough egg membranes liquefy,
0:38:55 > 0:38:57and the young wriggle free.
0:38:58 > 0:39:02He has two pouches in his skin, one on each hip,
0:39:02 > 0:39:06and the tadpoles start to squirm into them.
0:39:15 > 0:39:18Competition between the tadpoles is intense,
0:39:18 > 0:39:22for there are more of them than he can accommodate in his pouches.
0:39:47 > 0:39:52At last, he's taken on board as many as he can manage.
0:39:52 > 0:39:57He will now look after them for up to six weeks.
0:40:01 > 0:40:05The young remain in his pouches continuing their development,
0:40:05 > 0:40:08fuelled by the remains of the yolk in their infant stomachs.
0:40:14 > 0:40:18And then, one night, his behaviour changes.
0:40:20 > 0:40:22His flanks are rippling.
0:40:31 > 0:40:35The first of his young is emerging.
0:41:09 > 0:41:12The profound transformation
0:41:12 > 0:41:15that converted a tadpole into this young frog
0:41:15 > 0:41:20took place entirely within its father's moist pouch.
0:41:28 > 0:41:31The parched bush country of southern Africa.
0:41:31 > 0:41:37Here, it rains only twice a year, and then only briefly.
0:41:39 > 0:41:45But when it does, the ground, in places, erupts.
0:41:52 > 0:41:55Rain frogs, as they're aptly called,
0:41:55 > 0:41:59have been waiting for months below ground for this moment.
0:42:03 > 0:42:06After starving for so long, they're keen to feed.
0:42:38 > 0:42:43As darkness falls, the males begin to call.
0:42:43 > 0:42:45HIGH-PITCHED CHIRRUP
0:42:57 > 0:43:01Females are fat with eggs.
0:43:08 > 0:43:13The males are so much smaller that they can't embrace a female,
0:43:13 > 0:43:16so they produce glue from glands on their underside,
0:43:16 > 0:43:19and stick themselves to their partner's back.
0:43:22 > 0:43:26But sometimes, that only results in a chain of enthusiastic
0:43:26 > 0:43:29but undiscriminating males, stuck to one another.
0:43:37 > 0:43:40Their brief time above ground has come to an end.
0:43:40 > 0:43:43The female starts to dig.
0:43:44 > 0:43:48The diminutive male, being stuck on, goes with her.
0:43:48 > 0:43:52He will fertilise the eggs later, below ground.
0:43:59 > 0:44:03Her stay on the surface is over.
0:44:06 > 0:44:11The female has excavated a little chamber for herself,
0:44:11 > 0:44:13and below that she's made a second one,
0:44:13 > 0:44:16which she's filled with a frothy foam.
0:44:19 > 0:44:23This is the nursery for her tadpoles.
0:44:43 > 0:44:48The female stays underground, away from the lethal heat,
0:44:48 > 0:44:49for several more weeks.
0:44:59 > 0:45:05By now, her offspring have almost completed their time as tadpoles.
0:45:15 > 0:45:18The rains return.
0:45:23 > 0:45:27Below ground, the youngsters await their release.
0:45:46 > 0:45:49The female leads the way.
0:45:49 > 0:45:53And her brood are with her.
0:46:22 > 0:46:25Rain is even rarer in Australia.
0:46:25 > 0:46:29There, in the central deserts, it may not fall for years on end.
0:46:32 > 0:46:35But there are amphibians even here.
0:46:35 > 0:46:38Little toads that remain underground,
0:46:38 > 0:46:42in a state of suspended animation, for years,
0:46:42 > 0:46:45just to take advantage of a few rainy days.
0:46:47 > 0:46:52After the rains have fallen, spadefoot toads all emerge together.
0:46:52 > 0:46:57They must feed and breed, if possible, before the sun rises.
0:47:03 > 0:47:06But the desert dries only too quickly,
0:47:06 > 0:47:09even after the heaviest of storms.
0:47:09 > 0:47:13Temperatures rise to 50 degrees centigrade.
0:47:13 > 0:47:15Now water will evaporate instantly.
0:47:15 > 0:47:18This is one of the hottest places on Earth.
0:47:21 > 0:47:25So the toads have to retreat, once again, below ground.
0:47:25 > 0:47:29The miracle is that they're here at all.
0:47:32 > 0:47:36A toad that can live in as parched a desert as this
0:47:36 > 0:47:41is impressive evidence of the versatility of the amphibians,
0:47:41 > 0:47:45the way they can adapt their behaviour and their anatomy
0:47:45 > 0:47:47to live so far away from water.
0:47:47 > 0:47:49But there's one group of animals
0:47:49 > 0:47:54that can really call the desert their own - the lizards.
0:47:54 > 0:47:59And we'll look at them in the next episode of Life In Cold Blood.
0:48:08 > 0:48:12Amphibians are the most threatened group of vertebrates on the planet.
0:48:12 > 0:48:14In recent years,
0:48:14 > 0:48:19a strange and lethal fungal disease has started to spread among them.
0:48:21 > 0:48:25The golden frog, which lives only in one small area in Panama,
0:48:25 > 0:48:27was in particular danger,
0:48:27 > 0:48:30as the disease is already on the frontier of its territory.
0:48:30 > 0:48:33If we were to film it at all, we would have to move quickly.
0:48:36 > 0:48:39For series producer Miles Barton,
0:48:39 > 0:48:42that meant cutting short Christmas.
0:48:54 > 0:48:56We had been told that in Panama,
0:48:56 > 0:48:59the frogs' few remaining breeding streams
0:48:59 > 0:49:03were being rapidly destroyed by the building of a new road,
0:49:03 > 0:49:07making the last tiny population even more at risk from the disease.
0:49:10 > 0:49:13The fungus clogs the animal's moist skin.
0:49:13 > 0:49:16Since all frogs breathe through their skin,
0:49:16 > 0:49:19infected animals die from suffocation.
0:49:21 > 0:49:24Frog biologist Erik Lindquist,
0:49:24 > 0:49:27who first described the golden frog's signalling behaviour,
0:49:27 > 0:49:30helped the film team to thoroughly disinfect their kit
0:49:30 > 0:49:33before travelling into the frogs' territory.
0:49:36 > 0:49:39Freshly scrubbed up, Erik took the team
0:49:39 > 0:49:42to one of the golden frog's last-known breeding sites.
0:49:47 > 0:49:50But would they still be there?
0:49:50 > 0:49:52DISTANT CROAK
0:49:52 > 0:49:54Yeah, you hear that? That's a male calling.
0:49:59 > 0:50:02We have another male crawling up over here,
0:50:02 > 0:50:04crawling up the rock face.
0:50:05 > 0:50:09But with the fungus approaching at a rate of up to 25 miles a year,
0:50:09 > 0:50:14the frogs were rapidly disappearing from all their known breeding sites.
0:50:14 > 0:50:17The advance crew immediately set about filming
0:50:17 > 0:50:20as much of the behaviour as they could.
0:50:28 > 0:50:30By the time I arrived,
0:50:30 > 0:50:34there was only one remaining location where the frogs survived.
0:50:40 > 0:50:43Where exactly are we going?
0:50:43 > 0:50:46I would prefer not saying, precisely.
0:50:46 > 0:50:49You see, this is really the last population of the golden frog
0:50:49 > 0:50:51left in the wild,
0:50:51 > 0:50:55and historically, the locals have been collecting out these animals
0:50:55 > 0:51:02as good luck talisman, and so now we're left with just one population.
0:51:02 > 0:51:08I'm concerned that if the secret locality gets given out,
0:51:08 > 0:51:12- there'll be international collectors that would come.- Really?
0:51:12 > 0:51:14Sure. They're rare enough now
0:51:14 > 0:51:20where many people would pay top dollar for these animals.
0:51:20 > 0:51:23Were they ever what you might call common?
0:51:23 > 0:51:25When I talk to people who have been here in the past,
0:51:25 > 0:51:30the populations were so abundant that one would have to watch where they're
0:51:30 > 0:51:32stepping to keep from killing one.
0:51:32 > 0:51:33- Really?- Yes, yes.
0:51:35 > 0:51:38Erik has his own low-tech method of finding them,
0:51:38 > 0:51:40which he assures me normally works.
0:51:44 > 0:51:47LOW WHISTLING
0:51:50 > 0:51:53See, when you call, sometimes they'll call back
0:51:53 > 0:51:56and they'll reveal their locations.
0:51:56 > 0:51:58Sometimes they're tucked away behind leaves
0:51:58 > 0:52:00and they're really difficult to find.
0:52:00 > 0:52:02Hopefully we can elicit a response.
0:52:02 > 0:52:05HE WHISTLES
0:52:08 > 0:52:11It's the fastest way to get them to shut up.
0:52:15 > 0:52:16- Was that him?- Yeah, listen.
0:52:20 > 0:52:22- So they're here?- They're here.
0:52:22 > 0:52:24There's one over there.
0:52:29 > 0:52:33See him right there. Looks like a male.
0:52:33 > 0:52:34Make him do it again.
0:52:34 > 0:52:37HE WHISTLES
0:52:41 > 0:52:43FROG WHISTLES
0:52:44 > 0:52:47- You have to hum and whistle at the same time.- Can't do it!
0:52:47 > 0:52:49See if he can.
0:52:52 > 0:52:54HE TRIES TO WHISTLE
0:53:00 > 0:53:04Now we knew the frogs were still here, we could complete the filming.
0:53:06 > 0:53:09The local people have always treasured
0:53:09 > 0:53:11their remarkable little frog,
0:53:11 > 0:53:15but Erik was the first to document its signalling behaviour.
0:53:15 > 0:53:17It was an animal that was just walking.
0:53:17 > 0:53:20I wasn't sure if the animal was trying to flush out prey
0:53:20 > 0:53:24or if it was using it in a communication role.
0:53:24 > 0:53:26And so a group of us set out
0:53:26 > 0:53:29to look at whether or not this was communication.
0:53:29 > 0:53:32We tried mirror presentations to the animals.
0:53:32 > 0:53:34When you presented them with a mirror,
0:53:34 > 0:53:36they would hand-wave at the mirror
0:53:36 > 0:53:40as opposed to, say, the backside of a mirror that wasn't reflective.
0:53:41 > 0:53:45Some of us have looked specifically at an LCD screen,
0:53:45 > 0:53:50a little television with a hand-waving, semaphoring frog,
0:53:50 > 0:53:55and it has elicited a number of responses, specifically from males.
0:53:55 > 0:53:59What, you show a television picture to a male and he waves back?
0:53:59 > 0:54:03He waves back and he'll even call, to the male on the television screen.
0:54:03 > 0:54:05- Really?- It's really fascinating.
0:54:06 > 0:54:10They then experimented with a life-size plastic model,
0:54:10 > 0:54:12complete with waving arm,
0:54:12 > 0:54:17the sort of high-tech gear I thought I might manage to operate myself.
0:54:32 > 0:54:35It's not as easy as you might think.
0:54:40 > 0:54:42Erik showed me how it should be done.
0:54:42 > 0:54:47You've got to get that slow-motion wave just right.
0:54:49 > 0:54:52The frogs waved.
0:55:01 > 0:55:03They called.
0:55:05 > 0:55:08They even attacked.
0:55:08 > 0:55:12So that wave really is a form of communication.
0:55:12 > 0:55:16So they're just saying, "Keep off, keep off."
0:55:16 > 0:55:17Huh, is that right?
0:55:17 > 0:55:21We're not sure. Sometimes there seem to be certain hand waves
0:55:21 > 0:55:23that may indicate appeasement,
0:55:23 > 0:55:26showing that, "I'm just walking through, perhaps, your territory.
0:55:26 > 0:55:28"Don't bother me."
0:55:28 > 0:55:30Really? "Ah, please."
0:55:32 > 0:55:35But how endangered is the golden frog?
0:55:36 > 0:55:39This is it. What you see.
0:55:39 > 0:55:44You're going to be the last crew to film these in the wild.
0:55:45 > 0:55:47'And indeed we were.
0:55:47 > 0:55:49'Soon after finishing filming,
0:55:49 > 0:55:52'the local scientists decided the time had come
0:55:52 > 0:55:56'to take all the surviving golden frogs into captivity,
0:55:56 > 0:55:59'before the fungus arrives here and kills them all.
0:55:59 > 0:56:02'They and other rare species of frog also threatened
0:56:02 > 0:56:06'were being brought back to a special frog hospital,
0:56:06 > 0:56:08'where I was introduced to some of the other patients.'
0:56:08 > 0:56:10So what are these?
0:56:10 > 0:56:12They're nocturnal, so they spend...
0:56:12 > 0:56:15'Here, they're being treated daily with a fungicide.
0:56:15 > 0:56:17'But without a vaccine to protect them,
0:56:17 > 0:56:20'and with the fungus still at large in the forest,
0:56:20 > 0:56:23'they can't be re-introduced into their proper home.'
0:56:28 > 0:56:31Frogs, so common in these humid forests,
0:56:31 > 0:56:33are crucial links in the ecology.
0:56:33 > 0:56:37If they disappear, all kinds of food chains will be broken.
0:56:37 > 0:56:41The effect could be little short of catastrophic to wildlife in general.
0:56:44 > 0:56:45And sadly, for now at least,
0:56:45 > 0:56:50it seems that the golden frog has waved its last in the wild.
0:57:15 > 0:57:18Subtitles by Red Bee Media Ltd
0:57:29 > 0:57:32E-mail subtitling@bbc.co.uk