- "Circus bugs?! How can you be circus bugs?!"
- —Flik, finding out that the warrior bugs aren't who he thought they were
Flik first sees them in the city doing a Robin Hood act, believing them to be warriors, and they believe him to be a talent scout, and then convinces them to come to Ant Island to help him deal with the grasshoppers. They soon discover their misunderstandings, and are angry with Flik for not telling them about actually combating grasshoppers, and attempt to leave, but after a bird attacks them, during which they save Dot, and Francis's leg is broken, they decide to stay.
Later, P.T. Flea comes to Ant Island looking for them, and inadverently reveals the truth about them. The Queen and Princess Atta banish them from the island, along with Flik as punishment for lying to the colony. After Dot overhears a couple of grasshoppers talking about Hopper's scheme to squish the Queen, she goes after Flik and the circus bugs to tell them about the dire situation and convinces them to return. The circus bugs entertain Hopper and his gang while Flik and the blueberries pilot the fake bird they constructed to scare the grasshoppers; it works, until P.T. sets it on fire.
After seeing Thumper beat up Flik and hearing Hopper insult the colony and his troupe, P.T. realizes his mistake and teams up with the ants to defeat Hopper and his gang. Following Hopper's defeat, P.T. and his troupe spend the winter on Ant Island before returning to the circus in the spring, bringing a group of acrobatic ants and Hopper's younger brother Molt (now called "Tiny" and working as a strongman) with them, while promising to come back and visit in the future and receiving a fond farewell from the colony.
- Princess Atta: "You mean you're not warriors?"
P.T. Flea: "Are you kidding? These guys are the lousiest circus bugs you've ever seen, and they're gonna make me rich!"
- —Princess Atta, shocked to learn the truth about the Circus Bugs from P.T. Flea
The circus bugs consist of:
- P.T. Flea: Ringmaster
- Francis: Clown
- Slim: Clown
- Heimlich: Clown
- Dim: "Lion/Ferocious Beast"
- Rosie: "Lion-Tamer"
- Tuck and Roll: "Human" cannonballs
- Manny: Magician
- Gypsy: Manny's Lovely Assistant
- Molt ("Tiny"): Strongman
- Ants (about 8): Acrobats
- Fireflies: Lighting, Snacks, Setup
- Spider: Musician
- Millipedes: Travel
- The circus bugs made a cameo appearance as circus cars during the end credits of Cars.