The Whispering Death makes its first appearance in this episode.

What Flies Beneath
Season 1,riders of berk, Episode 14
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Air date February 6th, 2013
Written by Unknown
Directed by Unknown
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The episode begins with all the animals, while peacefully chewing grass, they are being pulled down mysteriously underground. The scene then shifts to Hiccup's bedroom, where Toothless is pacing, sniffing, looking around and giving low menacing growls with the reason yet unknown. Hiccup's narration is also given:

"Everybody have a past, even dragons. And sometimes the past can come back to haunt them. And when it does, you're gonna need to be there for them."

The next morning, a huge mysterious hole has been noticed by the Vikings, and Bucket had fallen inside it the previous night. Toothless, inwardly boiling with rage, comes towards the hole, and begins growling fiercely at it, and Hiccup tries to settle him down, saying that it was just a hole. Bucket reports that the hole looks very strange, in fact, he says that it looked like an underground village. Just then, something strikes Bucket, and he goes flying out of the hole. On being questioned by Stoick, Bucket says that something was down there, something big. Toothless, brooding over Bucket's claim, goes inside it and disappears into one of the many underground side tunnels.

The ground above starts shaking. After a few seconds, a very large dragon erupts of the hole, the Whispering Death. It looks at each of the Academy dragons with its white eyeballs (which doesn't have visible pupils), and dives back into the ground. Fishlegs says that the dragon they just saw was a 'Whispering Death'. This dragon has attracted Tuffnut, and he says that whatever it was, he wanted one, and it had a great name, even better than Hideous Zippleback. Then, the Whispering Death erupts out of the ground again. Gobber suggests to Hiccup that he try to calm or train it by touching its nose and feeding it grass. Hiccup asks Fishlegs for details about the Whispering Death. Fishlegs immediately replies that they are Boulder Class dragons, razor sharp teeth, incredibly strong, and hunts from underground. When Snotlout questions on how to deal with this thing, Stoick then appears on Thornado, saying that Thornado had something to say to this beast. But even Thornado's powerful roars didn't seem to affect the Whispering Death.

The Academy dragons follow Thornado to help him defeat it, but Toothless appears out of the hole, and roars at the other dragons, saying that this wasn't their battle. But since Toothless couldn't fly, the Whispering Death seemed to get the better of him. The wild dragon can see Toothless' tail and recognizes that he's been maimed, leaving him ground-bound. Toothless makes desperate attempts to fly, but it didn't work much to his obvious frustration.

Hiccup, on seeing this, decides to get on his back to help him fly to defeat the Whispering Death. But when Hiccup tries to get on him, Toothless halts him, much to the astonishment of Hiccup, and the rest of the gang. Toothless roars as if saying that it was a  fight between him and the Whispering Death, and he should not interfere in it. The Whispering Death releases a volley of spines and hits Toothless in the leg with one. Gobber begins launching a catapult at the Whispering Death, hitting it twice. Then suddenly when the sunlight falls on it, the dragon dives back to its hole.

Hiccup tends to Toothless' injured leg. Toothless seems normal now, and allows Hiccup to remove the spine. After removing, he quickly runs up and past the doors of the Great Hall, in the direction the Whispering Death retreated. Hiccup, Astrid, and Fishlegs are all still puzzled by Toothless' behavior, and the way he wanted to fight by himself. Snotlout even teases Hiccup about it, but Hiccup snaps back that it is not funny, and that Toothless could have been killed. As Toothless looks off toward where his attacker headed from his vantage point, Hiccup is sill worried about his increasingly erratic Night Fury.

The group asks Fishlegs what the Book of Dragons says about Whispering Death; they're from the boulder class, its specialty is obviously digging, it fires serrated spines from every inch of his body as well as rings of fire and has no known weakness. The group attempts to track Toothless and the Whispering Death through the forest, hoping to either find Toothless first and snap him back to his senses or find the Whispering Death and train it. Confronting the Whispering Death, Hiccup and Fishlegs chase him through the underground tunnels, getting up close and way too personal the group discover an old injury, a Night Fury bite mark. Putting two and two together Hiccup and Fishlegs realize that the Whispering Death and Toothless are old rivals and they now wish to challenge. Escaping the Whispering Death's tunnels the group is once again confronted by the wild dragon.

At first they attempt to calm him using Dragon nip but the dragon turns out to be allergic, not only sneezing away the Dragon nip but sneezing it into the other dragons causing them to fall unconscious. Luckily Toothless arrives on scene and continues the fight with his nemesis; none of the other dragons want to get involved realizing that what is going on is between the two of them.

The Whispering Death eventually backs Toothless onto a cliff and attempts to knock him to his death via fire rings. With Toothless being unable to fly, he was sure to be killed. Left with no other choice to help Toothless Hiccup jumps into the canyon, prompting Toothless to jump after him, allowing Hiccup to mount the dragon granting him flight. Now evenly matched the odds are further pushed into Toothless's favor with Fishlegs realizing that the Whispering Death can't stand bright light.

To this end the group chases the Whispering Death out of the tunnels by firing a fire blast by Toothless, pressing the advantage Hiccup and Toothless keep themselves in the sunlight blinding the Whispering Death and allowing Toothless to pin him down. Just when it seems like Toothless is about to permanently end the rivalry between the two dragons Hiccup stops him and the Whispering Death runs off.

As Hiccup and Toothless seal off the holes with rocks Hiccup narrates, commenting that when your past catches up with you, you'll need friends to back you up.